This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Errington, J.
Right arrow Articles by Scheffers, D.-J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Errington, J.
Right arrow Articles by Scheffers, D.-J.

 Previous Article  |  Next Article 

Microbiology and Molecular Biology Reviews, March 2003, p. 52-65, Vol. 67, No. 1
1092-2172/03/$08.00+0     DOI: 10.1128/MMBR.67.1.52-65.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Cytokinesis in Bacteria

Jeffery Errington,* Richard A. Daniel, and Dirk-Jan Scheffers

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom

SUMMARY
INTRODUCTION
SELECTION OF THE DIVISION SITE
    Nucleoid Occlusion
    The Min System
ASSEMBLY OF THE FtsZ RING
    Polymerization
    Mechanism of Constriction
    Asymmetric Division during Sporulation
    FtsA
MEMBRANE ANCHOR
    ZipA
    Equivalents of ZipA in Other Organisms?
SEPTAL PEPTIDOGLYCAN MACHINERY AND ASSOCIATED PROTEINS
    Complex and Diverse Assembly Pathways for Late Division Proteins?
    The Penicillin-Binding Protein FtsI
    FtsW
    FtsK
    FtsN
    FtsL/DivIC
    FtsQ/DivIB
CONSTRICTION AND CLOSURE OF THE DIVISION SEPTUM
THE FUTURE
ACKNOWLEDGMENTS
REFERENCES

arrow
SUMMARY
 
Work on two diverse rod-shaped bacteria, Escherichia coli and Bacillus subtilis, has defined a set of about 10 conserved proteins that are important for cell division in a wide range of eubacteria. These proteins are directed to the division site by the combination of two negative regulatory systems. Nucleoid occlusion is a poorly understood mechanism whereby the nucleoid prevents division in the cylindrical part of the cell, until chromosome segregation has occurred near midcell. The Min proteins prevent division in the nucleoid-free spaces near the cell poles in a manner that is beginning to be understood in cytological and biochemical terms. The hierarchy whereby the essential division proteins assemble at the midcell division site has been worked out for both E. coli and B. subtilis. They can be divided into essentially three classes depending on their position in the hierarchy and, to a certain extent, their subcellular localization. FtsZ is a cytosolic tubulin-like protein that polymerizes into an oligomeric structure that forms the initial ring at midcell. FtsA is another cytosolic protein that is related to actin, but its precise function is unclear. The cytoplasmic proteins are linked to the membrane by putative membrane anchor proteins, such as ZipA of E. coli and possibly EzrA of B. subtilis, which have a single membrane span but a cytoplasmic C-terminal domain. The remaining proteins are either integral membrane proteins or transmembrane proteins with their major domains outside the cell. The functions of most of these proteins are unclear with the exception of at least one penicillin-binding protein, which catalyzes a key step in cell wall synthesis in the division septum.


arrow
INTRODUCTION
 
Cell division in bacteria is effected by a complex macromolecular machinery containing seven or more conserved proteins, which assemble with a defined dependence hierarchy at the site of division. At the end of the process, two new cell poles have been formed, and so all of the cell envelope layers (including the membrane, wall, outer membrane, and S layer, if present) must be remodeled during division. Although the central players in division appear to be highly conserved, the diverse nature of bacterial cell envelopes clearly influences the precise pathway taken during division, so that some of the division proteins have specialized roles required only in certain groups of bacteria.

Many genes and proteins required for division have been defined by classical and molecular genetics. In the last few years, all of these proteins have been shown to be targeted to the division site and the dependence pathways for this assembly have been worked out in Escherichia coli and to a lesser extent in Bacillus subtilis (summarized in Tables 1 and 2) (25, 54). Disappointingly, despite these advances, clear biochemical functions have so far been elucidated for only two proteins. The first, FtsZ, is cytosolic and is present in virtually all eubacteria as well as in many eukaryotic organelles. It is a tubulin homologue and can polymerize, like tubulin, to form a ring-like structure (the Z ring) at the division site. The Z ring plays a key role in constriction of the cell membrane, as well as in coordination of the whole process of division. The second key biochemical activity required (for organisms with peptidoglycan [PG] cell walls), is a specialized penicillin-binding protein (PBP) required for synthesis of the wall material in the new cell poles.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Localization of cell division proteins to the division site in E. coli and their interdependences for localization


View this table:
[in this window]
[in a new window]
  		TABLE 2. Localization of cell division proteins to the division site in B. subtilis and their interdependences for localization

As a result of several decades of work, the following general steps in bacterial cell division can now be recognized: (i) selection of the division site, usually at midcell between the recently replicated and segregated nucleoids; (ii) assembly of cytoplasmic apparatus, almost invariably involving FtsZ and, in most organisms, also FtsA; these proteins can bind and hydrolyze nucleoside triphosphates, which may provide the energy to remodel the cell shape, possibly counteracting forces due to turgor and/or existing wall architecture; (iii) interaction with one or more proteins that provide a linkage to the cell membrane and potentially other cell envelope layers; (iv) assembly of proteins with major extracellular domains, particularly specialized PBPs, which direct synthesis of the wall material and other cell envelope layers that will constitute the new cell poles; and constriction and possibly an additional step of septum closure.

In the last few years, substantial progress has been made in several aspects of cell division, particularly the molecular basis for division site selection by the Min system, the pathway of assembly of the division protein machinery, the biochemistry of FtsZ polymerization, and, finally, the solution of the crystal structures of several division proteins. It is also becoming clear that although some aspects of the division machinery are highly conserved, other elements, particularly the later steps, have diverged significantly. The purpose of this review is to discuss the latest developments in the field of cell division and to describe the emerging distinctions in division processes of different organisms, particularly the paradigmatic gram-negative and gram-positive species, E. coli and B. subtilis, respectively. Various aspects of division have been discussed extensively in other recent, general reviews (19, 111, 112, 116, 146).


arrow
SELECTION OF THE DIVISION SITE
 
Formation of the Z ring is generally accepted to be a key event in the initiation of cell division. However, little is known about how the timing of ring assembly is regulated and about how the transition from ring assembly to constriction is controlled temporally. The simplest model at present is that the timing of ring assembly is a function of the mechanism of division site placement. There is an emerging consensus for two key factors involved in selection of the correct midcell site for cell division (reviewed in references 8, 74, and 117). One involves the chromosome itself, through an effect called nucleoid occlusion (129, 172). The second, termed the Min system, is responsible for specifically blocking the unwanted potential division sites at the cell poles (Fig. 1).



View larger version (40K):
[in this window]
[in a new window]
  		FIG. 1. Division site selection in rod-shaped bacteria. (A) Roles of nucleoid occlusion and the Min system. In cells that are about to divide, the correct midcell division site is chosen by the combined action of two negative regulatory systems. The localization of the two nucleoids blocks division in their vicinity, as shown, leaving spaces available for division at the correct midcell site and at the cell poles. The Min system acts to prevent incorrect division at the cell poles. (B) Blocking division at the cell poles. The MinCD inhibitor associates with the cytoplasmic membrane at the cell poles and prevents FtsZ polymerization. The C-terminal domain of MinC (CC) ensures MinC dimerization and interacts with MinD (D), which in turn associates with the membrane. The N-terminal domain of MinC (CN) interacts with FtsZ (Z) and prevents polymerization of FtsZ or interaction of other cell division proteins with the FtsZ ring (see the text). The MinD-MinC stoichiometry, and the presumed action of MinC, preventing the formation of correct FtsZ interactions remains hypothetical. (C and D) Contrasting functioning of the Min system in E. coli (C) and B. subtilis (D). MinD (chevrons [ATP form] and rectangles [ADP form]) is postulated to polymerize in the presence of ATP. In E. coli (A), it forms dynamic filaments emanating from one cell pole. A ring of MinE proteins associates with the ends of the filaments and moves in a poleward manner, by interaction with the MinD filaments. MinE stimulates hydrolysis of ATP by MinD, and this results in the release of monomers, probably following a conformational change (rectangles), which enter the cytoplasm. After exchange of the ADP for ATP, MinD polymers can re-form at the opposite cell pole, possibly requiring a nucleation site at the pole. In B. subtilis (B), MinD forms static filaments restricted to the polar zones as a result of nucleation by DivIVA protein targeted to the cell poles (black triangles). In both cases, MinD is associated with the division inhibitor (MinC; not shown), which blocks Z ring formation. Reproduced reference 8 with permission from the publisher.

Nucleoid Occlusion

The still poorly defined mechanism of nucleoid occlusion was revealed by the observation that cell division was found to be largely inhibited in the vicinity of the nucleoid of cells in which DNA replication and/or segregation was perturbed (129). In normal (rod-shaped) cells that are about to divide, there are three sites where DNA is absent or reduced in concentration (Fig. 1A). One lies at midcell, between the replicated and segregated chromosomes; the others lie at the cell poles. In principle, the midcell site appears and disappears cyclically, in parallel with rounds of chromosome replication. If the model is correct, bacteria have developed a mechanism that senses the presence of a DNA-free zone at midcell. Importantly, because the DNA-free zone is generated only toward the end of the DNA replication cycle, it could provide not only a spatial signal but also a temporal signal for division. In its original form, this model was based on the notion that the presence of an actively replicating nucleoid inhibited cell wall synthesis in its immediate vicinity. More recently, it has generally been reinterpreted in terms of a mechanism that prevents assembly of the Z ring in the vicinity of the nucleoid. The model has been tested in both E. coli and B. subtilis. Although there are reports indicating that Z rings can form directly over the nucleoid, these rings appear to form at positions where the DNA concentration is low compared to wild-type situations (27, 66, 145, 160). This suggests that it is not the presence of DNA per se but the concentration of DNA that is important (74), which is supported by the observation that in both E. coli and B. subtilis, Z rings can assemble before chromosome segregation is complete (42, 173).

Unfortunately, the mechanistic basis for nucleoid occlusion is poorly understood, and further understanding is hampered by difficulties in defining the precise locations of the boundaries of the rather diffuse nucleoid, in identifying the moment of replication termination in individual cells, and in understanding the forces that drive segregation (i.e., separation) of sister replicated chromosomes.

The Min System

A second form of regulation of the position of the Z ring is exerted by the min system, so called because mutants give rise to minicells through inappropriate division at the cell poles. In E. coli, the min system consists of three proteins, MinC, MinD, and MinE, which prevent cell division at the poles (recently reviewed in references 74 and 117). MinC and MinD act together as a negative regulator of FtsZ ring assembly, MinCD (41). MinC is the actual inhibitor of Z ring formation and prevents the localization of FtsZ and ZipA when overproduced (16, 87, 103, 119, 137). Furthermore, E. coli MinC inhibits FtsZ polymer assembly in vitro (87).

MinC is a dimer consisting of two distinct domains connected by a flexible linker (29) (Fig. 1B). The N-terminal domain, which interacts with FtsZ (85), shows some homology to FtsA and SpoIIAA (29). It is tempting to propose that MinC and FtsA have a similar mechanism of interaction with FtsZ. The similarity to SpoIIAA is intriguing because this protein interacts with the SpoIIE protein, which in turn has a direct interaction with FtsZ (see below). The C-terminal domain of MinC mediates dimerization (29, 85, 161) as well as the interaction with MinD (85). The crystal structures of MinC (29) and MinD (30, 78) revealed no information about the MinC-MinD interaction, but mutagenesis data point to a role for residues surrounding the MinD nucleotide-binding site in MinD-MinC interaction (78). MinD is a membrane-associated ATPase (39), which sequesters MinC to the membrane (39) (Fig. 1B). The MinCD complex probably has some additional affinity for assembling septal structures (90). The crystal structures of MinD from two different archaeal species revealed a monomeric protein with a fold typical of a large family of nucleotide-binding proteins (30, 78). MinE imparts topological specificity to the MinCD inhibitor by preventing it from working at midcell (40). MinE is a dimeric protein with two separate domains: an N-terminal anti-MinCD domain (139, 178) and a C-terminal topological specificity-dimerization domain (96, 139, 177, 178). The structure of the latter domain clearly showed how MinE dimerizes, and mutagenesis identified two key residues in MinE localization, but the interaction with MinCD remains to be resolved (97).

In the past few years, fluorescence imaging has provided important new insights into the organization of the Min system. Remarkably, the MinCD inhibitor oscillates from pole to pole, with a periodicity of about 20 s (84, 142, 143) (Fig. 1C). MinE forms a band that also oscillates, but with a more restricted pattern, moving from side to side about midcell. Each sideways movement seems to be involved in sweeping MinCD from the cell pole; this is followed by reassembly of a MinCD cap at the opposite pole (59, 71). MinC seems to be a passive player, simply moving with MinD (84, 142). Experiments with spherical mutants of E. coli suggest that the Min system can help to identify the long axis of the cell, thereby promoting division parallel to this long axis (28). This could explain the presence of a Min system in various gram-negative cocci (116), which on the face of it do not have an overt polarity.

Recently, Lutkenhaus and coworkers have made considerable progress in understanding the molecular basis for oscillation (Fig. 1C). First they showed that MinD ATPase activity is strongly stimulated by MinE in the presence of phospholipid vesicles. Moreover, MinE mutant proteins affected in their stimulation of MinD ATPase showed equivalent effects on the periodicity of MinD oscillation in vivo (86). These authors went on to demonstrate that MinD binds to the phospholipid vesicles, distorting the vesicles into tubular structures coated with MinD. The MinD was probably polymerized in a helical array with a pitch of 59 Å, similar to the length of the long axis of the MinD monomer determined by X-ray crystallography (83). These results strongly suggested that the MinCD inhibitor forms a polymerized structure at the membrane with MinD in the ATP-bound form, which is displaced from the membrane by interaction with MinE. They also suggested that MinE works by stimulating ATP hydrolysis and release of MinD from the membrane. After nucleotide exchange in the cytosol, MinCD binds to the membrane in the MinE-free zone in the other cell half (86). This model is supported by computer simulations that can faithfully reproduce the oscillation patterns of the system in silico (121).

The components of the Min system are distributed unequally among bacteria. Although MinD-like proteins are present across a broad range of species, MinC is less highly conserved and MinE is even more restricted in its distribution (116). The Min system of B. subtilis has been extensively characterized. Clear homologues of MinC and MinD are present, but there is no MinE (102). The function of MinE in topological control of MinCD activity is provided by a quite different protein, DivIVA (24, 48) (Fig. 1D). DivIVA is stably associated with the cell poles, and it recruits MinCD to the cell poles, probably by a direct interaction with MinD (49, 120). The zone occupied by MinD appears to spread out from the pole more than that of DivIVA, again suggesting a cooperative self-interaction of MinD, which is perhaps nucleated at the pole by DivIVA. DivIVA-MinCD remains associated with the newly formed poles after division, thereby preventing future division at those sites (48, 119, 120). Thus, even though B. subtilis uses a homologous MinCD system to block polar division, topological control over MinCD is exerted in a strikingly different manner from that in E. coli. Various other bacterial species, particularly gram-positive cocci, lack the Min system altogether (117), and certain clostridia appear to possess both MinE and DivIVA (157), raising interesting questions about how division site selection occurs in these organisms.


arrow
ASSEMBLY OF THE FtsZ RING
 
FtsZ is arguably the most critical component of the division machinery for several reasons. First, it is the most widely conserved, being present in virtually all eubacteria and most archaea and in the organelles of many eukaryotes (115). Second, it is at the top of the hierarchy of assembly of division proteins — in general, all other division proteins require FtsZ for targeting to the division site (Tables 1 and 2). Third, certain ftsZ mutations that alter the form of the Z ring in the cell, for example producing helical structures, have a similar effect on the gross morphology of cell division (5).

Polymerization

The Z ring almost certainly consists of FtsZ polymers because these can readily be formed in vitro, in the presence of GTP, under a range of conditions. FtsZ polymers strongly resemble tubulin protofilaments (20, 51, 107, 108, 126). The simultaneous elucidation of the structures of FtsZ from the thermophilic archaeon Methanococcus jannaschii (105) and the {alpha}ß-tubulin heterodimer from bovine brain (133) provided conclusive evidence that FtsZ and tubulin are homologues (164). The great overall structural similarity between FtsZ and tubulin is described in detail elsewhere (131). Recent biochemical data show that not only is there great structural homology between FtsZ and tubulin but also that their polymerization mechanisms are similar. GTP hydrolysis is activated by a cation-coordinating loop (T7) that inserts into the nucleotide-binding site of an adjacent monomer (128, 150, 151). Nucleotide hydrolysis is immediate on polymerization, and the hydrolyzed phosphate is not released immediately (149). This points to an important role for phosphate release in FtsZ polymer dynamics. In tubulin, the {gamma}-phosphate of GTP is sensed by loop T3 (132); in FtsZ, this loop is displaced depending on whether GDP or GTP is bound to the protein (45). Polymer stability is likely to be conferred by a GTP cap at one end of the FtsZ polymer, as may be inferred from the observation that FtsZ can be stabilized by the addition of nonhydrolyzable GTP-{gamma}-S that does not exchange for most of the nucleotide that is bound to the polymer (152) and from the observation that FtsZ polymers rapidly disassemble after the addition of GDP (128, 152). Although the longitudinal interactions in the FtsZ polymer and microtubules appear very similar, the lateral interactions found in microtubules are not evident, based on the FtsZ crystal structure (106, 132). Nevertheless, this question remains to be fully resolved because FtsZ appears to be capable of forming various types of polymers, with different types of lateral arrangement, particularly in the presence of divalent cations (see, e.g., references 107 and 108).

In vivo, Z rings can both form and disassemble rapidly, on a timescale of 1 to 3 min for assembly and 1 min for disassembly (3, 159). Recently, Stricker et al. (158) used fluorescence recovery after photobleaching to show that the Z ring is highly dynamic throughout its existence. They also showed that about 30% of cellular FtsZ is present in the Z ring and that the FtsZ in the Z ring readily exchanges with FtsZ in the cytosol. The speed of exchange of protein subunits in the ring and the rate of GTP hydrolysis showed a good correlation (158). Combined with the in vitro data on FtsZ polymerization (described above), a model can be envisaged in which the Z ring is made up of a meshwork of filaments that undergoes continuous rapid exchange with a pool of short FtsZ polymers formed in the cytosol (158).

Mechanism of Constriction

As mentioned above, the orientation of the Z ring seems to determine the location of the division plane. The results with both the ftsZ26 mutant, which makes helical Z rings and septa, and of rodA mutants, which grow as a sphere instead of a rod, show that constriction does not require closure of a complete FtsZ ring (5). "Purse string" type models for constriction can therefore probably be excluded. Several models for Z ring constriction have been described (reviewed in reference 19). (All of these models require the presence of an anchor to connect FtsZ to the membrane [discussed below].) In the first model, short filaments of FtsZ slide relative to one another, aided by an as yet unidentified motor protein, to reduce the circumference of the ring. In the second model, FtsZ filaments lose subunits through depolymerization at an anchor site (which must somehow remain attached to the filament end), again resulting in ring constriction. The observation that overproduction of FtsZ inhibits constriction of the FtsZ ring (169), which can be explained by the inhibition of depolymerization through the concentration increase, lends support to this model. In a third model, constriction is effected by bending of FtsZ filaments, resulting from the conformational change that occurs on hydrolysis of GTP to GDP (108) or release of Pi. More sophisticated in vitro reconstitution systems are probably needed to test these models. Moreover, although FtsZ is a ubiquitous, key player in division, models for constriction will ultimately have to incorporate the functions of the various other division proteins that have been identified.

Asymmetric Division during Sporulation

A key event during sporulation in B. subtilis is the formation of an asymmetric division septum at one of the cell poles. This asymmetric septum formation is preceded by a change of localization of the Z ring from midcell to the cell poles (100) followed by localization of other division proteins and the sporulation-specific FtsZ-associated protein SpoIIE (recently reviewed in reference 54 (see below). The switch in FtsZ localization was previously thought to be effected by a mechanism which blocked formation of the Z ring at midcell and released the inhibition of polar septation (9, 100). However, recently Ben-Yehuda and Losick (14) showed that a medial Z ring can be converted into, or replaced by, a helical FtsZ filament that grows outward toward the cell poles, where it is then converted into bipolar Z rings. Both FtsA and EzrA were shown to colocalize with the FtsZ helical structures. The switch from midcell to polar Z rings was shown to be driven by a combination of increased cellular concentration of FtsZ and the presence of sporulation protein SpoIIE (14).

Helical FtsZ structures have previously been observed in misshapen vegetative cells of B. subtilis (91) and in E. coli cells that overproduce FtsZ (113, 159) or that lack the membrane phospholipid phosphatidylethanolamine (123). This suggests that the ability to form such structures is a general property of FtsZ proteins and even raises the possibility that the general form of the Z ring at division sites may actually comprise a helix of very short pitch (14).

FtsA

FtsA is the only known cell division protein, other than FtsZ, that lacks a clear membrane-spanning sequence. The FtsA primary sequence places it in the actin/Hsp70/sugar kinase ATPase superfamily (17). The crystal structure of FtsA from Thermotoga maritima was recently solved (165) and confirmed the similarity to actin, except for the absence of the 1B domain of actin and the presence of a novel domain dubbed 1C. Generally, however, FtsA is typical of the actin superfamily (17), possessing two domains with a common core and an interdomain cleft harboring the nucleotide-binding site. The significance of the structural similarity to actin is not clear. Although FtsA does not appear to polymerize in vitro, B. subtilis FtsA has recently been shown to dimerize and to bind and hydrolyze ATP (56). There is evidence that E. coli FtsA can be phosphorylated (148), but phosphorylation has not been observed with B. subtilis FtsA (A. Feucht, personal communication), and the molecular consequences of phosphorylation of E. coli FtsA are not clear.

As shown in Table 1, FtsA assembles at the Z ring early. This is due to a direct interaction between the two proteins, as demonstrated by yeast two-hybrid interaction studies. The extreme C terminus of FtsZ seems to be the site of interaction, as for other interactions (see below) (Fig. 1B) (46, 114, 174). Two particular residues in the E. coli FtsZ C terminus, L372 and the highly conserved P375 (50), are critical for its interaction with FtsA. Interestingly, although there is a clear overall homology between FtsZ and tubulin, the C termini of both proteins are quite different (although both are highly acidic). The C-terminal tail of FtsZ is highly conserved in bacteria, with a central Pro-X-(Phe/hydrophobic residue) motif (50), which mediates the interaction with both FtsA and ZipA.

In E. coli, the cellular ratio of FtsA to FtsZ is 1:100, this ratio is important for correct division (31, 44). This has important implications for the nature of the FtsZ-FtsA interaction in vivo because there is not sufficient FtsA to form a complete ring and it presumably makes only widely interspersed contacts with FtsZ filaments. FtsA dimerization could allow it could cross-link adjacent FtsZ filaments. Interestingly, the level of FtsA appears to be much higher in B. subtilis; with an intracellular FtsA-to-FtsZ ratio of 1:5 (56). Given the distribution of both FtsZ and ZipA in ring-associated and non-ring-associated fractions and their dynamics (158; see below), the actual stoichiometry in the division complex may differ significantly from the ratios measured by quantitative immunoblotting. Ultimately, one specific role for FtsA is recruitment of other cell division proteins to the division site (Tables 1 and 2). In principle, it is possible that FtsA uses the energy of ATP hydrolysis to drive assembly. Alternatively, the ATP hydrolysis could in some way help to power cell constriction.


arrow
MEMBRANE ANCHOR
 
As mentioned above, all current models for FtsZ ring constriction require the ring to be tightly bound to the membrane. Moreover, membrane association is clearly required to coordinate membrane invagination, with synthesis of septal PG. Several candidates for the putative membrane anchor of the Z ring exist. One set of candidates would be the PBPs or proteins involved in recruiting the PBP complex to the septum (see below). However, these proteins are recruited to the division complex at a relatively late step in the hierarchy (see below). The best current candidate is a protein that assembles early in the division cycle, ZipA (Fig. 1B).

ZipA

ZipA was identified in E. coli by affinity blotting for FtsZ-interacting proteins (69). It is a membrane protein with an unusual membrane topology in which the N-terminal membrane anchor is followed by a large cytoplasmic portion that consists of two clear domains connected by a Pro-Gln rich flexible tether (134) (Fig. 2A). Although ZipA is essential for division in E. coli, its primary sequence is poorly conserved, and obvious ZipA homologues have been reported only for Haemophilus influenzae (144). ZipA localizes to the Z ring in an FtsZ-dependent, FtsA-independent manner, and overexpression of zipA abolishes cell division (69, 70, 104) (Table 1). Interestingly, FtsZ rings are formed in the presence of either ZipA or FtsA but not in the absence of both proteins (138), so that these proteins play a partially redundant role in Z ring assembly, although both are needed for septal constriction (Fig. 2A; Table 1). Increased zipA expression suppresses the thermosensitivity of the ftsZ84(Ts) mutant through FtsZ ring stabilization, and purified ZipA stabilizes both FtsZ and FtsZ84 polymers in vitro (144). Polymers formed in the presence of ZipA show enhanced bundling (72, 144), similar to FtsZ polymers that have been stabilized with divalent cations (127). The bundling of FtsZ protofilaments could be important in formation of the macroscopic Z ring. Additionally, or alternatively, bundling could enhance the stability of individual FtsZ protofilaments through a reduction of GTPase activity (P. A. J. de Boer, personal communication).



View larger version (44K):
[in this window]
[in a new window]
  		FIG. 2. Organization of the cell division apparatus during various steps in the division process. A comparison of the E. coli system (A and C) with that of B. subtilis (B and D) is shown. Numbers beside proteins indicate the hierarchy of assembly; a question mark indicates that this is not yet clear. (A and B) Formation of the Z ring and anchoring of the Z ring to the membrane. FtsZ (Z) interacts with the cytoplasmic cell division protein FtsA (A) via the C-terminal tail of Z, which is flexible. FtsA (at least of B. subtilis [56]) is a dimer. In E. coli, the FtsZ ring is anchored to the membrane, at least partly, by ZipA (ZA), which also binds to the flexible C-terminal FtsZ tail. In most bacteria, functional equivalents of ZipA have not yet been found. In B. subtilis, EzrA protein has a similar topology to ZipA, although it is not essential for division. (C and D) Assembly of the remainder of the cell division machinery. In E. coli (C), the hierarchy for assembly of the remaining proteins is essentially linear, as numbered, except for FtsL (L) and YgbQ (Y). The other proteins are labeled according to their fts suffix. In B. subtilis (D), there is no apparent homologue of FtsN and the FtsK homologue (SpoIIIE) is not required for division. The DivIB (IB), DivIC (C), FtsL (L), and PBP-2B (I) proteins assemble in a concerted manner. The order of assembly of FtsW (W) is not known.

Various lines of evidence have shown that it is the C-terminal domain of ZipA that interacts with FtsZ and is responsible for the enhanced bundling observed in vitro (72, 104, 124, 125). As with FtsA, ZipA binds to the extreme C terminus of FtsZ (72, 73). The structure of the C-terminal domain of ZipA containing the C-terminal 17 residues of FtsZ revealed a split ß-{alpha}-ß motif with the FtsZ peptide bound in a shallow, hydrophobic, solvent-exposed cavity that runs the width of the ZipA C-terminal domain (124, 125). A major portion of the FtsZ fragment is in contact with ZipA residues, mainly through hydrophobic interactions but also via two hydrogen bonds (124). Interestingly, the highly conserved Pro residue of the C-terminal tail of FtsZ does not contact ZipA. Various other methods have been applied to characterize FtsZ residues implicated in the ZipA interaction, yielding unequivocal results. A surface plasmon resonance analysis of a peptide comprising the C-terminal 17 FtsZ residues and the C-terminal ZipA domain identified D373, I374, F377 and L378 as the most critical FtsZ residues (124). In an in vivo assay, an L378A mutant interacted with ZipA whereas D373A, I374A, and F377A mutants did not (114). Finally, in a yeast two-hybrid assay, a D373G mutant did not bind ZipA (73).

The nature of the interaction between FtsZ and ZipA is clearly well established in vitro. In vivo, ZipA is 10- to 100-fold less abundant than FtsZ (69), and only about 30% of total ZipA localizes to the division site (158). Strikingly, ZipA displays a dynamic behavior similar to that of FtsZ, with a constant exchange of protein between the Z ring and an external pool, in this case located in the membrane rather than the cytosol, as analyzed by fluorescence recovery after photobleaching (158) (H. P. Erickson, personal communication). An intriguing question is whether the observed dynamics of FtsZ and ZipA (158) reflects the movement of both proteins individually or of FtsZ-ZipA complexes.

As with FtsA (see above), the low abundance of ZipA means that it can interact with only a small proportion of FtsZ subunits. Moreover, even though FtsA and ZipA both interact with the C-terminal tail of FtsZ, they probably do not compete for binding sites on the same FtsZ molecules.

Equivalents of ZipA in Other Organisms?

In B. subtilis, EzrA was identified as a negative regulator of FtsZ polymerization (98). In an ezrA null mutant, the critical concentration for formation of the Z ring was lowered, with polar ring formation that could overcome the effects of minCD overexpression, suggesting that EzrA acts to destabilize FtsZ polymers (103). The gene is conserved in several gram-positive bacteria. Although the phenotype of an ezrA mutant is, on the face of it, the opposite of the zipA phenotype, the two proteins share the unusual membrane topology mentioned above for ZipA. Thus, the predicted EzrA protein also has a single N-terminal membrane span and a large cytoplasmic domain (98) (Fig. 2B). Since ZipA and EzrA have similar topologies (although there is no significant primary sequence similarity) and interact with FtsZ to promote or destabilize polymers, it seems possible that the proteins are functionally homologous; however, more work is needed to substantiate this idea.

Also in B. subtilis, as mentioned above, a membrane-bound protein, SpoIIE, is implicated in the shift of cell division to polar sites that occurs when this organism initiates sporulation (52, 100). SpoIIE is made specifically during sporulation and is targeted to the division site in an FtsZ-dependent manner (6, 100, 101). Targeting does not require later division proteins encoded by divIB, divIC, or ftsL (55, 101). Although polar Z rings and septa are made in the absence of SpoIIE, they are delayed and substantially reduced in frequency (57, 95). SpoIIE has 10 transmembrane spans at its N terminus (domain 1), a linker domain of about 250 residues (domain 2), and a C-terminal domain involved in a quite separate regulatory function (52). SpoIIE interacts directly with FtsZ, probably through domain 2 (109), but the nature of this interaction and its function in vivo have not yet been elucidated. In principle, however, its role could be similar to that of ZipA in medial division of E. coli.

In addition to these proteins, it is conceivable that one or more of the transmembrane proteins involved in the synthesis of cell wall peptidoglycan could contribute to anchoring the Z ring to the membrane. So far, single mutations affecting these genes do not seem to prevent formation of the Z ring, although, as described below, several more transmembrane proteins are required for constriction of the ring.


arrow
SEPTAL PEPTIDOGLYCAN MACHINERY AND ASSOCIATED PROTEINS
 
Most of the remaining proteins involved in cell division have at least one membrane span and a substantial extracellular domain. Surprisingly, the only protein with a defined biochemical function is FtsI, which is required for septal peptidoglycan synthesis. In principle, the other division proteins could simply be involved in directing the PG-synthesizing machinery (FtsI plus various other proteins) to the division site, or they could have other functions, such as an active involvement in PG synthesis or a role in the membrane dynamics associated with invagination.

Complex and Diverse Assembly Pathways for Late Division Proteins?

The assembly pathways for the late, membrane-bound division proteins have been extensively analyzed in both E. coli and B. subtilis. These experiments have revealed surprising differences between the two organisms. In E. coli, the dependence pathway for assembly is, with one recent exception (22), completely linear (Table 1; Fig. 2C), with the sequence FtsK -> FtsQ -> [FtsL YgbQ] -> FtsW -> FtsI -> FtsN. Thus, FtsK requires none of the other proteins to assemble at the Z ring, whereas FtsN depends on all of the other proteins. Brackets indicate that localization of FtsL and localization of YgbQ are codependent. In contrast, the equivalent proteins of B. subtilis appear to be recruited in a much more concerted manner (Table 2; Fig. 2D) (54). DivIB, DivIC, FtsL, PBP-2B, and probably FtsW (R. A. Daniel and L. J. Wu, unpublished data) are all completely interdependent for assembly at the division site; mutation or depletion of any of the proteins prevents all of the others from assembling. Although it is satisfying to have established the details of these dependence pathways, they shed little light on the mechanisms of division; however, in E. coli at least, they provide indications of where to look for specific protein-protein interactions.

The next sections summarize what is known about the functions and interactions of these proteins in E. coli and B. subtilis.

The Penicillin-Binding Protein FtsI

As mentioned above, septation requires a dedicated PBP for synthesis of the PG forming the new poles of the daughter cells. An extensive and diverse family of proteins involved in the final stages of PG synthesis have been identified on the basis of their ability to bind penicillins (reviewed recently in reference 65). Many bacteria have multiple PBPs, and there appears to be considerable redundancy in the way they function (43, 141). The high-molecular-weight (class A) PBPs (e.g., PBP-1a of E. coli and PBP-1 of B. subtilis) typically possess both transglycosylase and transpeptidase activity and seem to be involved in general PG synthesis (65). Class B PBPs are somewhat smaller and have only transpeptidase activity (65). In E. coli, two members of this class of protein appear to play important, spatially specialized roles in PG synthesis. Mutations in the mrdA gene (encoding PBP-2) give a characteristic round-cell phenotype, apparently as a result of a loss of ability to synthesize PG in the cylindrical part of the cell (155). In contrast, mutation of the ftsI or pbpB gene (encoding PBP-3) abolishes PG synthesis during division but still support cell elongation (156).

Functional homologues of FtsI (PBP-3) are recognizable both by their amino acid sequence and by the conserved position of their gene within a cluster of genes involved in division and cell wall synthesis, in many diverse bacteria. In B. subtilis, the equivalent gene (also called pbpB and encoding PBP-2B) is required for septation (35, 175).

The FtsI proteins have, in their N-terminal 50 or so residues, a noncleavable transmembrane span. This is followed by a domain of about 200 amino acids (aa) of poorly understood function (the non-penicillin-binding [nPB] domain) and then by a C-terminal domain of about 300 aa, which contains the characteristic sequence motifs representing the catalytic residues of PBPs (the penicillin-binding [PB] domain) (65). In an attractive current model for PG synthesis, in gram-negative bacteria at least, FtsI acts in a multiprotein complex that introduces three new glycan strands in parallel with hydrolysis of an existing docking or template strand (82). Full details of how FtsI fits into this complex remain to be determined. The crystal structure of the extracellular part of the equivalent protein from Streptococcus (PBP-2X) was determined several years ago (135). The PB domain shows the expected fold for the catalytic portion of a transpeptidase. The nPB domain has an interesting "sugar tongs" structure, with the legs of the tongs projecting away from the PB domain and the head of the tongs embedded into the side of the PB domain. Site-directed mutagenesis of the nPB domain resulted in the isolation of some mutations that destabilize the protein, suggesting that the nPB domain may behave as an intramolecular chaperone, required for proper folding of the PB domain (64, 118). However, other explanations are possible, including a site for interaction with other division proteins or proteins of the general PG synthetic machinery. It is even possible that this domain plays a direct role in PG synthesis: some of the mutants do not significantly affect catalysis, as judged by penicillin binding, but it is possible that they are unable to act on more physiologically relevant substrates.

It is generally thought that the class A PBPs of E. coli are nonspecialized, being equally involved in both cylindrical-wall and septal PG synthesis. However, in B. subtilis the major class A PBP, PBP-1, encoded by the ponA gene, is partially targeted to septal sites, and on depletion of the protein, the most prominent effect is on cell division (136). This again might again reflect differences in the way PG synthesis is organized in gram-positive and -negative organisms.

Nanninga's group has obtained evidence for the existence of a penicillin-insensitive enzymatic step in PG synthesis at the onset of septal constriction (130). However, so far, the putative enzyme responsible for this function has not been identified.

FtsW

FtsW is a member of the SEDS family of proteins (for "shape, elongation, division, and sporulation") (81, 88). These proteins appear to have 10 transmembrane spans (60) and are frequently encoded by a gene that lies close to the gene for a class B PBP. Thus, in E. coli, ftsW lies in the same operon as ftsI (18, 89) and mrdB (encoding SEDS protein RodA) lies adjacent to mrdA (encoding PBP-2) (162). In both cases, the phenotype obtained when the SEDS-encoding gene is knocked out is similar to that obtained when its cognate PBP-encoding gene is knocked out. In B. subtilis, the gene in the equivalent position to ftsW of E. coli, spoVE, is specialized for sporulation (80). However, a functional homologue of ftsW (ylaO) has been found elsewhere in the genome (81) (Daniel and Wu, unpublished). According to a survey of sequenced bacterial genomes (116), there is a perfect presence-absence correlation between FtsW and FtsI, suggesting that their functions are intimately connected. The most likely function for the SEDS proteins, apart from targeting their cognate PBPs, would seem to be translocation of the lipid-linked precursor for PG synthesis from the inside to the outside of the membrane and delivery to its cognate PG-synthesizing complex (82). Such a role would be consistent with the multiple transmembrane structure of these proteins. However, the class B PBP has no transglycosylase activity and so is unlikely to be the immediate recipient for the precursor. Presumably, at least one class A PBP needs to be involved. Why should different substrate translocation proteins be required? There is some evidence that the transpeptidase activities of PBP-2 and FtsI have different substrate preferences, with the former preferring a pentapeptide side chain and the latter preferring a tripeptide side chain (13). Perhaps, RodA and FtsW have different precursor affinities and channel the appropriate precursor to differentiated PG-synthesizing machineries containing their cognate class B PBPs (82).

Although a role for FtsW in stabilization of FtsZ has been suggested for E. coli, no further evidence for a direct FtsZ-FtsW interaction has been reported. Interestingly, Datta et al. (38) have recently reported an FtsZ-FtsW interaction in Mycobacterium tuberculosis, mediated by a prominent C-terminal extension to FtsW, which is absent from the homologues of most other bacteria.

FtsK

FtsK is a large protein with several distinct roles in the late stages of cell division. It has a large soluble cytoplasmic domain that is required for chromosome segregation (53) and is highly conserved almost throughout the eubacteria. This is separated, by an extremely variable linker, from an N-terminal membrane domain containing four membrane spans. In E. coli (but not B. subtilis), the N-terminal domain is essential for division. The original temperature-sensitive mutations affecting the N-terminal domain of FtsK caused a late block in division (12), but protein depletion experiments have subsequently demonstrated an early block (25, 47, 167). Interestingly, the late-blocking ftsK(Ts) mutations (but not the depletion mutations) could be suppressed by deletion of dacA, which codes for carboxypeptidase PBP5 (47). Draper et al. (47) speculated that the late stages of septation could require a PBP with a preference for pentapeptide side chains, which should be enhanced in the absence of PBP5. In contrast, all of the ftsK mutations were suppressed by overexpression of ftsN (47; see below).

The C-terminal domain of FtsK is capable of ATP-dependent translocation along DNA, consistent with a role in pumping DNA through a closing septum (7). This behavior is similar to the DNA translocation activity displayed by the B. subtilis FtsK homologue SpoIIIE, which ensures proper chromosome translocation into the prespore compartment of sporulating cells (10). Moreover, the C-terminal domain of FtsK promotes Xer recombination reactions, required to resolve chromosome dimers before chromosome segregation (7). Given these functions of the FtsK C-terminal domain during the final steps of DNA replication and segregation, it is conceivable that FtsK helps to ensure that division occurs only in the region between newly replicated chromosomes.

FtsN

The ftsN gene was isolated as a multicopy suppressor of a temperature-sensitive ftsA mutation (32). Surprisingly, it also suppressed, to a greater or lesser extent, temperate-sensitive mutations in the ftsI, ftsQ, and ftsK genes (32). The protein has an N-terminal transmembrane segment that directs the major C-terminal domain to the periplasmic side of the membrane, but this segment can be replaced by heterologous sequences, even a cleavable signal peptide, suggesting that its division-specific function is contained in the C-terminal domain (33). The protein is poorly conserved, with clear homologues present only in enteric bacteria and Haemophilus spp. (33). However, FtsN shows weak sequence similarity to cell wall amidases (for example, Cw1C and SpoIIB in B. subtilis), suggesting a possible role in wall hydrolysis. Conceivably, FtsN could be required to cleave certain bonds in the wall to allow initiation of constriction. The suppressor activity of FtsN overproduction could work by further weakening the wall in such a way that a partially nonfunctional division machinery (e.g., one containing thermosensitive mutations affecting FtsA, FtsQ, or FtsI [32]) can operate more normally.

FtsL/DivIC

FtsL of E. coli is a small (121-aa) transmembrane protein with poorly conserved primary sequence (67, 163). The only potentially informative sequence feature is a coiled-coil motif in its major extracellular (C-terminal) domain (67). Such domains are typically involved in protein-protein interactions (110). Little is known about the function of FtsL in division, except that there is biochemical support for self-interaction through the detection of protein dimers (61). Originally, two temperature-sensitive alleles of ftsL were isolated: one produced filaments at the nonpermissive temperature, whereas the other caused lysis (163). The significance of this is not clear. B. subtilis appears to have a functional homologue of FtsL. Although the primary sequence similarity is negligible, the protein is a likely homologue on the grounds of similar size and predicted transmembrane topology, division phenotype, and the location of its gene immediately upstream of pbpB (36, 37). Mutagenesis of the B. subtilis ftsL gene lent support to the notion that few if any of its residues are critical for function (153) and therefore that its function is more likely to be structural than catalytic.

B. subtilis has a second ftsL-like gene, divIC, which is also required for division (99). It appears that DivIC and FtsL interact to form a heterodimer or -oligomer, on the basis of both yeast two-hybrid experiments and native gel electrophoresis (154). Furthermore, depletion of FtsL results in degradation of DivIC, indicating that formation of an FtsL-DivIC complex could stabilize DivIC (36). Interestingly, FtsL (of B. subtilis) is itself an intrinsically unstable protein (34). It is possible that FtsL plays an important regulatory role in division, because septation is shut down very rapidly if the gene is turned off (36). One important factor controlling FtsL turnover in B. subtilis is DivIB protein (34), as described below. Recently, a new essential cell division gene, ygbQ, was identified in Vibrio cholerae and E. coli (22). Depletion of the protein gave a filamentous phenotype typical of other cell division mutants. The YgbQ protein is a small transmembrane protein with a predicted structure similar to that of FtsL and DivIC. The protein localized to the division site, and this localization was codependent with FtsL. Although the protein was not significantly similar to any protein of B. subtilis, it did show weak but significant similarity to the DivIC protein of Bacillus halodurans. Taken together, these properties strongly point to YgbQ being homologous to DivIC.

FtsQ/DivIB

FtsQ of E. coli is a 276-aa protein of low abundance (~22 copies per cell [23]) with a similar transmembrane topology to FtsL, FtsN, and FtsI (23, 75). The gene appears essential for division in E. coli, but its precise function is unclear (26). The ftsQ gene lies immediately upstream of ftsA and ftsZ in a range of organisms, but the overall sequence conservation is again poor. B. subtilis has a probable homologue of ftsQ called divIB (11, 76), but some of the properties of DivIB highlight possible differences in function. First, as with FtsA (see above), DivIB appears to be much more abundant (about 100-fold more) than its E. coli counterpart (147). Second, mutants with null mutations of divIB are viable, although they are temperature sensitive and fail to divide at higher temperatures (11). The likely basis for temperature-sensitive division was recently illuminated through the finding that the division defect can be largely overcome by overexpression of ftsL (34). Therefore, the main division function of DivIB could be to protect FtsL from degradation at higher temperatures. Interestingly, the dependence of DivIC stability on FtsL appears to be mediated in some way by DivIB, because in the absence of DivIB, DivIC stability is no longer dependent on FtsL (R. A. Daniel, unpublished data). All of these effects point to the formation of one or more complexes between these proteins. Recent results from this laboratory suggest that the target for these effects could be the PG-synthesizing machinery, because divIB null mutants can be suppressed by mutations affecting the nPB module of FtsI (Daniel, unpublished). This would support the notion that one important role of the nPB domain of FtsI is assembly of the septum-specific PG-synthesizing machinery at the division site.


arrow
CONSTRICTION AND CLOSURE OF THE DIVISION SEPTUM
 
The final steps of cell division pose a number of interesting questions, most of which remain to be resolved. During constriction, the assembled proteins described in the previous sections coordinately organize the annular constriction of the cytoplasmic membrane, cell wall, and any other cell envelope layers present, such as the outer membrane of gram-negative bacteria. E. coli and B. subtilis appear to be strikingly different in the mechanics of this process. In E. coli, division proceeds by gradual constriction of the cylindrical part of the cell, whereas in B. subtilis, a new cross-wall is formed with no concomitant constriction of the existing cylinder. One important consequence of this latter scheme is that the initial product of division is a pair of sister cells that are sealed off from each other by a double membrane but joined by a layer of wall material. Cell separation occurs later by the action of various cell wall autolysins (58). The distinction between these processes was recently blurred by the finding that a combination of mutations inactivating two autolytic enzymes results in E. coli cells that divide via a septum-like structure, with delayed cell separation (79).

Constriction is presumably an energy-dependent process. There are at least two potential drivers. One is constriction of the cytosolic Z ring, with associated factors and membrane anchor (see above). The other is inward growth of an annulus of PG. Indirect support for the first mechanism comes from the similarity of FtsZ and FtsA to eukaryotic cytoskeletal proteins (tubulin and actin). Moreover, the ability of certain wall-less organisms to divide suggests that PG synthesis is not essential for division, although there could be an equivalent extracellular mechanism substituting for PG synthesis in these organisms. Interestingly, the FtsZ ring is missing from chlamydiae. Although these organisms do not have a full PG wall, they retain the proteins needed for most steps in PG synthesis (63). Intriguingly, they do not appear to have a PBP with transglycosylase activity, but they retain several class B PBPs, including one closely related to FtsI (63). In principle, this could allow them to make a peptide-based polymer that substitutes in part for PG (63).

Insights into the possible interplay between the FtsZ and PG components of the division machinery of B. subtilis came from the effects of depletion of PBP 2B (FtsI) (35). As expected, inhibition of cell division occurs, giving rise to filamentous cells. The filaments can assemble Z rings at regularly spaced intervals, but none of the extracellular proteins (FtsL, DivIB, and DivIC) are recruited. However, at about the midpoint of many of the filaments, a complete assembly of division proteins is formed. These assemblies probably depend on residual PBP-2B activity giving rise to some septal PG synthesis. Interestingly, complete invagination of a pair of septal membranes occurs at many of these sites with little or no concomitant septal PG synthesis. This shows that septal membrane invagination probably needs a little PG synthesis to initiate but that, once started, it can largely be disengaged from PG synthesis (35). Conceivably, the major distortion of membrane conformation that is needed when ingrowth of the septum starts is an energetic barrier to initiation. A small annulus of newly synthesized PG at the division site could be sufficient to stabilize the distortion in the membrane, after which membrane invagination can readily proceed to completion.

During division, most of the proteins involved appear to be gradually lost from the division site as this process progresses and the diameter of the septal annulus decreases. Very little is known about how the complex division apparatus accommodates changes in the diameter of the annulus.

Finally, a specialized form of PG synthesis might be required to insert a small circular disk of wall material at the centre of the septum. Certain temperature-sensitive mutations, notably those of the ftsK gene, appear to result in arrest of division with deep invaginations of the septum, consistent with this idea (12).


arrow
THE FUTURE
 
Cell division is one of the most central processes in biology. For no cellular system do we have a clear idea of the molecular mechanisms underlying this process. However, for bacteria, particularly E. coli and B. subtilis, we have reached the point where most, if not all, of the essential players have been identified and the hierarchy with which they are assembled at the Z ring has been worked out. Furthermore, the crystal structures of most of the players will soon be available and the sites of some protein-protein interactions have been characterized. Of the five steps described in the Introduction, significant progress has been made in understanding the first four, which really comprise the assembly of the machinery. The major challenges now lie in understanding how the assembled machinery is triggered into action and how it shrinks and disassembles as the annulus closes, as discussed in the preceding section. Some progress is being made toward understanding the regulation of FtsZ polymerization in vitro. Ultimately, however, progress in understanding the molecular details of division may be limited by the availability of new experimental methods that allow in vitro reconstruction of more complete versions of the division apparatus.


arrow
ACKNOWLEDGMENTS
 
This work was supported by a grant from the BBSRC. J.E. gratefully acknowledges receipt of a BBSRC Senior Research Fellowship. D-J.S. is supported by a Marie-Curie postdoctoral fellowship (HPMF-CT-2001-01421) of the European Union.

We are grateful to Harold P. Erickson and Piet A. J. de Boer for helpful comments and communication of unpublished data.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom. Phone: 44 1865 275561. Fax: 44 1865 275556. E-mail: jeff.errington{at}path.ox.ac.uk. Back


arrow
REFERENCES
 
    1
  1. Addinall, S. G., E. Bi, and J. Lutkenhaus. 1996. FtsZ ring formation in fts mutants. J. Bacteriol. 178:3877-3884.[Abstract/Free Full Text]
    2. 2
  2. Addinall, S. G., C. Cao, and J. Lutkenhaus. 1997. FtsN, a late recruit to the septum in Escherichia coli. Mol. Microbiol. 25:303-309.[CrossRef][Medline]
    3. 3
  3. Addinall, S. G., C. Cao, and J. Lutkenhaus. 1997. Temperature shift experiments with an ftsZ84(Ts) strain reveal rapid dynamics of FtsZ localization and indicate that the Z ring is required throughout septation and cannot reoccupy division sites once constriction has initiated. J. Bacteriol. 179:4277-4284.[Abstract/Free Full Text]
    4. 4
  4. Addinall, S. G., and J. Lutkenhaus. 1996. FtsA is localized to the septum in an FtsZ-dependent manner. J. Bacteriol. 178:7167-7172.[Abstract/Free Full Text]
    5. 5
  5. Addinall, S. G., and J. Lutkenhaus. 1996. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol. 22:231-237.[CrossRef][Medline]
    6. 6
  6. Arigoni, F., K. Pogliano, C. D. Webb, P. Stragier, and R. Losick. 1995. Localization of protein implicated in establishment of cell type to sites of asymmetric division. Science 270:637-640.[Abstract/Free Full Text]
    7. 7
  7. Aussel, L., F. X. Barre, M. Aroyo, A. Stasiak, A. Z. Stasiak, and D. Sherratt. 2002. FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108:195-205.[CrossRef][Medline]
    8. 8
  8. Autret, S., and J. Errington. 2001. Dynamic proteins in bacteria. Dev. Cell 1:10-11.[CrossRef][Medline]
    9. 9
  9. Barák, I., P. Prepiak, and F. Schmeisser. 1998. MinCD proteins control the septation process during sporulation of Bacillus subtilis. J. Bacteriol. 180:5327-5333.[Abstract/Free Full Text]
    10. 10
  10. Bath, J., L. J. Wu, J. Errington, and J. C. Wang. 2000. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290:995-997.[Abstract/Free Full Text]
    11. 11
  11. Beall, B., and J. Lutkenhaus. 1989. Nucleotide sequence and insertional inactivation of a Bacillus subtilis gene that affects cell division, sporulation, and temperature sensitivity. J. Bacteriol. 171:6821-6834.[Abstract/Free Full Text]
    12. 12
  12. Begg, K. J., S. J. Dewar, and W. D. Donachie. 1995. A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177:6211-6222.[Abstract/Free Full Text]
    13. 13
  13. Begg, K. J., A. Takasuga, D. H. Edwards, S. J. Dewar, B. G. Spratt, H. Adachi, T. Ohta, H. Matsuzawa, and W. D. Donachie. 1990. The balance between different peptidoglycan precursors determines whether Escherichia coli cells will elongate or divide. J. Bacteriol. 172:6697-6703.[Abstract/Free Full Text]
    14. 14
  14. Ben-Yehuda, S., and R. Losick. 2002. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257-266.[CrossRef][Medline]
    15. 15
  15. Bi, E., and J. Lutkenhaus. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-164.[CrossRef][Medline]
    16. 16
  16. Bi, E., and J. Lutkenhaus. 1993. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J. Bacteriol. 175:1118-1125.[Abstract/Free Full Text]
    17. 17
  17. Bork, P., C. Sander, and A. Valencia. 1992. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl. Acad. Sci. USA 89:7290-7294.[Abstract/Free Full Text]
    18. 18
  18. Boyle, D. S., M. M. Khattar, S. G. Addinall, J. Lutkenhaus, and W. D. Donachie. 1997. ftsW is an essential cell-division gene in Escherichia coli. Mol. Microbiol. 24:1263-1273.[CrossRef][Medline]
    19. 19
  19. Bramhill, D. 1997. Bacterial cell division. Annu. Rev. Cell Dev. Biol. 13:395-424.[CrossRef][Medline]
    20. 20
  20. Bramhill, D., and C. M. Thompson. 1994. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl. Acad. Sci. USA 91:5813-5817.[Abstract/Free Full Text]
    21. 21
  21. Buddelmeijer, N., M. E. Aarsman, A. H. Kolk, M. Vicente, and N. Nanninga. 1998. Localization of cell division protein FtsQ by immunofluorescence microscopy in dividing and nondividing cells of Escherichia coli. J. Bacteriol. 180:6107-6116.[Abstract/Free Full Text]
    22. 22
  22. Buddelmeijer, N., N. Judson, D. Boyd, J. J. Mekalanos, and J. Beckwith. 2002. YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site. Proc. Natl. Acad. Sci. USA 99:6316-6321.[Abstract/Free Full Text]
    23. 23
  23. Carson, M. J., J. Barondess, and J. Beckwith. 1991. The FtsQ protein of Escherichia coli: membrane topology, abundance, and cell division phenotypes due to overproduction and insertion mutations. J. Bacteriol. 173:2187-2195.[Abstract/Free Full Text]
    24. 24
  24. Cha, J.-H., and G. C. Stewart. 1997. The divIVA minicell locus of Bacillus subtilis. J. Bacteriol. 179:1671-1683.[Abstract/Free Full Text]
    25. 25
  25. Chen, J. C., and J. Beckwith. 2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol Microbiol 42:395-413.[CrossRef][Medline]
    26. 26
  26. Chen, J. C., D. S. Weiss, J.-M. Ghigo, and J. Beckwith. 1999. Septal localization of FtsQ, an essential cell division protein in Escherichia coli. J. Bacteriol. 181:521-530.[Abstract/Free Full Text]
    27. 27
  27. Cook, W. R., and L. I. Rothfield. 1999. Nucleoid-independent identification of cell division sites in Escherichia coli. J. Bacteriol. 181:1900-1905.[Abstract/Free Full Text]
    28. 28
  28. Corbin, B. D., X. C. Yu, and W. Margolin. 2002. Exploring intracellular space: function of the Min system in round-shaped Escherichia coli. EMBO J 21:1998-2008.[CrossRef][Medline]
    29. 29
  29. Cordell, S. C., R. E. Anderson, and J. Lowe. 2001. Crystal structure of the bacterial cell division inhibitor MinC. EMBO J 20:2454-2461.[CrossRef][Medline]
    30. 30
  30. Cordell, S. C., and J. Löwe. 2001. Crystal structure of the bacterial cell division regulator MinD. FEBS Lett. 492:160-165.[CrossRef][Medline]
    31. 31
  31. Dai, K., and J. Lutkenhaus. 1992. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol 174:6145-6151.[Abstract/Free Full Text]
    32. 32
  32. Dai, K., Y. Xu, and J. Lutkenhaus. 1993. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J. Bacteriol. 175:3790-3797.[Abstract/Free Full Text]
    33. 33
  33. Dai, K., Y. Xu, and J. Lutkenhaus. 1996. Topological characterization of the essential Escherichia coli cell division protein FtsN. J Bacteriol 178:1328-1334.[Abstract/Free Full Text]
    34. 34
  34. Daniel, R. A., and J. Errington. 2000. Intrinsic instability of the essential cell division protein FtsL of Bacillus subtilis and a role for DivIB protein in FtsL turnover. Mol. Microbiol. 36:278-289.[CrossRef][Medline]
    35. 35
  35. Daniel, R. A., E. J. Harry, and J. Errington. 2000. Role of penicillin-binding protein PBP 2B in assembly and functioning of the division machinery of Bacillus subtilis. Mol. Microbiol. 35:299-311.[CrossRef][Medline]
    36. 36
  36. Daniel, R. A., E. J. Harry, V. L. Katis, R. G. Wake, and J. Errington. 1998. Characterization of the essential cell division gene ftsL (yllD) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol. Microbiol. 29:593-604.[CrossRef][Medline]
    37. 37
  37. Daniel, R. A., A. M. Williams, and J. Errington. 1996. A complex four-gene operon containing essential cell division gene pbpB in Bacillus subtilis. J. Bacteriol. 178:2343-2350.[Abstract/Free Full Text]
    38. 38
  38. Datta, P., A. Dasgupta, S. Bhakta, and J. Basu. 2002. Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J Biol Chem 277:24983-24987.[Abstract/Free Full Text]
    39. 39
  39. de Boer, P. A. J., R. E. Crossley, A. R. Hand, and L. I. Rothfield. 1991. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10:4371-4380.[Medline]
    40. 40
  40. de Boer, P. A. J., R. E. Crossley, and L. I. Rothfield. 1989. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641-649.[CrossRef][Medline]
    41. 41
  41. de Boer, P. A. J., R. E. Crossley, and L. I. Rothfield. 1992. Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J. Bacteriol. 174:63-70.[Abstract/Free Full Text]
    42. 42
  42. Den Blaauwen, T., N. Buddelmeijer, M. E. Aarsman, C. M. Hameete, and N. Nanninga. 1999. Timing of FtsZ assembly in Escherichia coli. J. Bacteriol. 181:5167-5175.[Abstract/Free Full Text]
    43. 43
  43. Denome, S. A., P. K. Elf, T. A. Henderson, D. E. Nelson, and K. D. Young. 1999. Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J. Bacteriol. 181:3981-3993.[Abstract/Free Full Text]
    44. 44
  44. Dewar, S. J., K. J. Begg, and W. D. Donachie. 1992. Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J. Bacteriol. 174:6314-6316.[Abstract/Free Full Text]
    45. 45
  45. Diaz, J. F., A. Kralicek, J. Mingorance, J. M. Palacios, M. Vicente, and J. M. Andreu. 2001. Activation of cell division protein FtsZ. Control of switch loop T3 conformation by the nucleotide {gamma}-phosphate. J. Biol. Chem. 276:17307-17315.[Abstract/Free Full Text]
    46. 46
  46. Din, N., E. M. Quardokus, M. J. Sackett, and Y. V. Brun. 1998. Dominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol. Microbiol. 27:1051-1063.[CrossRef][Medline]
    47. 47
  47. Draper, G. C., N. McLennan, K. Begg, M. Masters, and W. D. Donachie. 1998. Only the N-terminal domain of FtsK functions in cell division. J. Bacteriol. 180:4621-4627.[Abstract/Free Full Text]
    48. 48
  48. Edwards, D. H., and J. Errington. 1997. The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol. Microbiol. 24:905-915.[CrossRef][Medline]
    49. 49
  49. El Karoui, M., and J. Errington. 2001. Isolation and characterization of topological specificity mutants of minD in Bacillus subtilis. Mol. Microbiol. 42:1211-1221.[CrossRef][Medline]
    50. 50
  50. Erickson, H. P. 2001. The FtsZ protofilament and attachment of ZipA—structural constraints on the FtsZ power stroke. Curr. Opin. Cell Biol. 13:55-60.[CrossRef][Medline]
    51. 51
  51. Erickson, H. P., D. W. Taylor, K. A. Taylor, and D. Bramhill. 1996. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologues of tubulin polymers. Proc. Natl. Acad. Sci. USA 93:519-523.[Abstract/Free Full Text]
    52. 52
  52. Errington, J. 2001. Septation and chromosome segregation during sporulation in Bacillus subtilis. Curr. Opin. Microbiol. 4:660-666.[CrossRef][Medline]
    53. 53
  53. Errington, J., J. Bath, and L. J. Wu. 2001. Bacterial DNA transport. Nat. Rev. Mol. Cell. Biol. 2:538-545.[CrossRef][Medline]
    54. 54
  54. Errington, J., and R. A. Daniel. 2001. Cell division during growth and sporulation, p. 97-109. In L. Sonenshein, R. Losick, J. A. Hoch, (ed.), Bacillus subtilis and its relatives: from genes to cells. American Society for Microbiology, Washington, D.C.
    55. 55
  55. Feucht, A., R. A. Daniel, and J. Errington. 1999. Characterization of a morphological checkpoint coupling cell-specific transcription to septation in Bacillus subtilis. Mol. Microbiol. 33:1015-1026.[CrossRef][Medline]
    56. 56
  56. Feucht, A., I. Lucet, M. D. Yudkin, and J. Errington. 2001. Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol. Microbiol. 40:115-125.[CrossRef][Medline]
    57. 57
  57. Feucht, A., T. Magnin, M. D. Yudkin, and J. Errington. 1996. Bifunctional protein required for asymmetric cell division and cell-specific transcription in Bacillus subtilis. Genes Dev. 10:794-803.[Abstract]
    58. 58
  58. Foster, S. J., and D. L. Popham. 2001. Structure and synthesis of cell wall, spore cortex, teichoic acids, S-layers, and capsules, p. 21-41. In L. Sonenshein, R. Losick, and J. A. Hoch (ed.), Bacillus subtilis and its relatives: from genes to cells. American Society for Microbiology, Washington, D.C.
    59. 59
  59. Fu, X., Y.-L., Shih, and L. I. Rothfield. 2001. The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc. Natl. Acad. Sci. USA 98:980-985.[Abstract/Free Full Text]
    60. 60
  60. Gerard, P., T. Vernet, and A. Zapun. 2002. Membrane topology of the Streptococcus pneumoniae FtsW division protein. J Bacteriol 184:1925-1931.[Abstract/Free Full Text]
    61. 61
  61. Ghigo, J.-M., and J. Beckwith. 2000. Cell division in Escherichia coli: role of FtsL domains in septal localization, function, and oligomerization. J. Bacteriol. 182:116-129.[Abstract/Free Full Text]
    62. 62
  62. Ghigo, J.-M., D. S. Weiss, J. C. Chen, J. C. Yarrow, and J. Beckwith. 1999. Localization of FtsL to the Escherichia coli septal ring. Mol. Microbiol. 31:725-737.[CrossRef][Medline]
    63. 63
  63. Ghuysen, J.-M., and C. Goffin. 1999. Lack of cell wall peptidoglycan versus penicillin sensitivity: new insights into the chlamydial anomaly. Antimicrob. Agenets Chemother. 43:2339-2344.[Free Full Text]
    64. 64
  64. Goffin, C., C. Fraipont, J. Ayala, M. Terrak, M. Nguyen-Distèche, and J. M. Ghuysen. 1996. The non-penicillin-binding module of the tripartite penicillin-binding protein 3 of Escherichia coli is required for folding and/or stability of the penicillin-binding module and the membrane-anchoring module confers cell septation activity on the folded structure. J. Bacteriol. 178:5402-5409.[Abstract/Free Full Text]
    65. 65
  65. Goffin, C., and J. M. Ghuysen. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.[Abstract/Free Full Text]
    66. 66
  66. Gullbrand, B., and K. Nordström. 2000. FtsZ ring formation without subsequent cell division after replication runout in Escherichia coli. Mol. Microbiol. 36:1349-1359.[CrossRef][Medline]
    67. 67
  67. Guzman, L.-M., J. J. Barondess, and J. Beckwith. 1992. FtsL, an essential cytoplasmic membrane protein involved in cell division in Escherichia coli. J. Bacteriol. 174:7716-7728.[Medline]
    68. 68
  68. Hale, C. A., and P. A. de Boer. 2002. ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J. Bacteriol. 184:2552-2556.[Abstract/Free Full Text]
    69. 69
  69. Hale, C. A., and P. A. J. De Boer. 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88:175-185.[CrossRef][Medline]
    70. 70
  70. Hale, C. A., and P. A. J. De Boer. 1999. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J. Bacteriol. 181:167-176.[Abstract/Free Full Text]
    71. 71
  71. Hale, C. A., H. Meinhardt, and P. A. de Boer. 2001. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 20:1563-1572.[CrossRef][Medline]
    72. 72
  72. Hale, C. A., A. C. Rhee, and P. A. J. de Boer. 2000. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182:5153-5166.[Abstract/Free Full Text]
    73. 73
  73. Haney, S. A., E. Glasfeld, C. Hale, D. Keeney, Z. He, and P. de Boer. 2001. Genetic analysis of the Escherichia coli FtsZ.ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J. Biol. Chem. 276:11980-11987.[Abstract/Free Full Text]
    74. 74
  74. Harry, E. J. 2001. Bacterial cell division: regulating Z-ring formation. Mol. Microbiol. 40:795-803.[CrossRef][Medline]
    75. 75
  75. Harry, E. J., B. J. Stewart, and R. G. Wake. 1993. Characterization of mutations in divIB of Bacillus subtilis and cellular localization of the DivIB protein. Mol. Microbiol. 7:611-621.[CrossRef][Medline]
    76. 76
  76. Harry, E. J., and R. G. Wake. 1989. Cloning and expression of a Bacillus subtilis division initiation gene for which a homolog has not been identified in another organism. J. Bacteriol. 171:6835-6839.[Abstract/Free Full Text]
    77. 77
  77. Harry, E. J., and R. G. Wake. 1997. The membrane-bound cell division protein DivIB is localized to the division site in Bacillus subtilis. Mol. Microbiol. 25:275-283.[CrossRef][Medline]
    78. 78
  78. Hayashi, I., T. Oyama, and K. Morikawa. 2001. Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J. 20:1819-1828.[CrossRef][Medline]
    79. 79
  79. Heidrich, C., M. F. Templin, A. Ursinus, M. Merdanovic, J. Berger, H. Schwarz, M. A. de Pedro, and J. V. Holtje. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178.[CrossRef][Medline]
    80. 80
  80. Henriques, A. O., H. De Lencastre, and P. J. Piggot. 1992. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie 74:735-748.[CrossRef][Medline]
    81. 81
  81. Henriques, A. O., P. Glaser, P. J. Piggot, and C. P. Moran, Jr. 1998. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28:235-247.[CrossRef][Medline]
    82. 82
  82. Höltje, J. V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.[Abstract/Free Full Text]
    83. 83
  83. Hu, Z., E. P. Gogol, and J. Lutkenhaus. 2002. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. USA 99:6761-6766.[Abstract/Free Full Text]
    84. 84
  84. Hu Z., and J. Lutkenhaus. 1999. Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol. Microbiol. 34:82-90.[CrossRef][Medline]
    85. 85
  85. Hu Z., and J. Lutkenhaus. 2000. Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J. Bacteriol. 182:3965-3971.[Abstract/Free Full Text]
    86. 86
  86. Hu Z., and J. Lutkenhaus. 2001. Topological regulation of cell division in E. coli. Spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol. Cell 7:1337-1343.[CrossRef][Medline]
    87. 87
  87. Hu Z., A. Mukherjee, S. Pichoff, and J. Lutkenhaus. 1999. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. USA 96:14819-14824.[Abstract/Free Full Text]
    88. 88
  88. Ikeda M., T. Sato, M. Wachi, H. K. Jung, F. Ishino, Y. Kobayashi, and M. Matsuhashi. 1989. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 171:6375-6378.[Abstract/Free Full Text]
    89. 89
  89. Ishino, F., H. K. Jung, M. Ikeda, M. Doi, M. Wachi, and M. Matsuhashi. 1989. New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division. J. Bacteriol. 171:5523-5530.[Abstract/Free Full Text]
    90. 90
  90. Johnson, J. E., L. L. Lackner, and P. A. de Boer. 2002. Targeting of (D)MinC/MinD and (D)MinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J. Bacteriol. 184:2951-2962.[Abstract/Free Full Text]
    91. 91
  91. Jones, L. J. F., R. Carballido-Lopez, and J. Errington. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-922.[CrossRef][Medline]
    92. 92
  92. Katis, V. L., E. J. Harry, and R. G. Wake. 1997. The Bacillus subtilis division protein DivIC is a highly abundant membrane-bound protein that localizes to the division site. Mol. Microbiol. 26:1047-1055.[CrossRef][Medline]
    93. 93
  93. Katis, V. L., R. G. Wake, and E. J. Harry. 2000. Septal localization of the membrane-bound division proteins of Bacillus subtilis DivIB and DivIC is codependent only at high temperatures and requires FtsZ. J. Bacteriol. 182:3607-3611.[Abstract/Free Full Text]
    94. 94
  94. Khattar, M. M., S. G. Addinall, K. H. Stedul, D. S. Boyle, J. Lutkenhaus, and W. D. Donachie. 1997. Two polypeptide products of the Escherichia coli cell division gene ftsW and a possible role for FtsW in FtsZ function. J. Bacteriol. 179:784-793.[Abstract/Free Full Text]
    95. 95
  95. Khvorova, A., L. Zhang, M. L. Higgins, and P. J. Piggot. 1998. The spollE locus is involved in the Spo0A-dependent switch in the location of FtsZ rings in Bacillus subtilis. J. Bacteriol. 180:1256-1260.[Abstract/Free Full Text]
    96. 96
  96. King, G. F., S. L. Rowland, B. Pan, J. P. Mackay, G. P. Mullen, and L. I. Rothfield. 1999. The dimerization and topological specificity functions of MinE reside in a structurally autonomous C-terminal domain. Mol. Microbiol. 31:1161-1169.[CrossRef][Medline]
    97. 97
  97. King, G. F., Y. L. Shih, M. W. Maciejewski, N. P. Bains, B. Pan, S. L. Rowland, G. P. Mullen, and L. I. Rothfield. 2000. Structural basis for the topological specificity function of MinE. Nat. Struct. Biol. 7:1013-1017.[CrossRef][Medline]
    98. 98
  98. Levin, P. A., I. G. Kurtser, and A. D. Grossman. 1999. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 96:9642-9647.[Abstract/Free Full Text]
    99. 99
  99. Levin, P. A., and R. Losick. 1994. Characterization of a cell division gene from Bacillus subtilis that is required for vegetative and sporulation septum formation. J. Bacteriol. 176:1451-1459.[Abstract/Free Full Text]
    100. 100
  100. Levin, P. A., and R. Losick. 1996. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes Devol. 10:478-488.[Abstract]
    101. 101
  101. Levin, P. A., and R. Losick, P. Stragier, and F. Arigoni. 1997. Localization of the sporulation protein SpoIIE in Bacillus subtilis is dependent upon the cell division protein FtsZ. Mol. Microbiol. 25:839-846.[CrossRef][Medline]
    102. 102
  102. Levin, P. A., and P. S. Margolis, P. Setlow, R. Losick, and D. Sun. 1992. Identification of Bacillus subtilis genes for septum placement and shape determination. J. Bacteriol. 174:6717-6728.[Abstract/Free Full Text]
    103. 103
  103. Levin, P. A., and R. L. Schwartz, and A. D. Grossman. 2001. Polymer stability plays an important role in the positional regulation of FtsZ. J. Bacteriol. 183: 5449-5452.[Abstract/Free Full Text]
    104. 104
  104. Liu, Z., A. Mukherjee, and J. Lutkenhaus. 1999. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol. 31:1853-1861.[CrossRef][Medline]
    105. 105
  105. Löwe J., and L. A. Amos. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203-206.[CrossRef][Medline]
    106. 106
  106. Löwe J., and L. A. Amos. 1999. Tubulin-like protofilaments in Ca2+-induced FtsZ sheets. EMBO J. 18:2364-2371.[CrossRef][Medline]
    107. 107
  107. Löwe, J., and L. A. Amos. 2000. Helical tubes of FtsZ from Methanococcus jannaschii. Biol. Chem. 381:993-999.[CrossRef][Medline]
    108. 108
  108. Lu, C., M. Reedy, and H. P. Erickson. 2000. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182:164-170.[Abstract/Free Full Text]
    109. 109
  109. Lucet, I., A. Feucht, M. D. Yudkin, and J. Errington. 2000. Direct interaction between the cell division protein FtsZ and the cell differentiation protein SpoIIE. EMBO J. 19:1467-1475.[CrossRef][Medline]
    110. 110
  110. Lupas, A. 1996. Coiled coils: new structures and new functions. Trends Biochem Sci. 21:375-382.[CrossRef][Medline]
    111. 111
  111. Lutkenhaus, J., and S. G. Addinall. 1997. Bacterial cell division and the Z ring. Annu. Rev. Biochem. 66:93-116.[CrossRef][Medline]
    112. 112
  112. Lutkenhaus, J., and E. Bi. 2001. Cell morphogenesis and division. Curr. Opin. Microbiol. 4:621-624.[CrossRef]
    113. 113
  113. Ma, X., D. W. Ehrhardt, and W. Margolin. 1997. Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc. Natl. Acad. Sci. USA 93:12998-13003.[Abstract/Free Full Text]
    114. 114
  114. Ma, X., and W. Margolin. 1999. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J. Bacteriol. 181:7531-7544.[Abstract/Free Full Text]
    115. 115
  115. Margolin, W. 2000. Organelle division: self-assembling GTPases caught in the middle. Curr. Biol. 10:328-330.[CrossRef]
    116. 116
  116. Margolin, W. 2000. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24:531-548.[CrossRef][Medline]
    117. 117
  117. Margolin, W. 2001. Spatial regulation of cytokinesis in bacteria. Curr. Opin. Microbiol. 4:647-652.[CrossRef][Medline]
    118. 118
  118. Marrec-Fairley, M., A. Piette, X. Gallet, R. Brasseur, H. Hara, C. Fraipont, J. M. Ghuysen, and M. Nguyen-Distèche. 2000. Differential functionalities of amphiphilic peptide segments of the cell-septation penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 37:1019-1031.[CrossRef][Medline]
    119. 119
  119. Marston, A. L., and J. Errington. 1999. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol. Microbiol. 33:84-96.[CrossRef][Medline]
    120. 120
  120. Marston, A. L., H. B. Thomaides, D. H. Edwards, M. E. Sharpe, and J. Errington. 1998. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Devl. 12:3419-3430.[Abstract/Free Full Text]
    121. 121
  121. Meinhardt, H., and P. A. de Boer. 2001. Pattern formation in Escherichia coli: A model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc. Natl. Acad. Sci. USA 98:14202-14207.[Abstract/Free Full Text]
    122. 122
  122. Mercer, K. L., and D. S. Weiss. 2002. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184:904-912.[Abstract/Free Full Text]
    123. 123
  123. Mileykovskaya, E., Q. Sun, W. Margolin, and W. Dowhan. 1998. Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. J. Bacteriol. 180:4252-4257.[Abstract/Free Full Text]
    124. 124
  124. Mosyak, L., Y. Zhang, E. Glasfeld, S. Haney, M. Stahl, J. Seehra, and W. S. Somers. 2000. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J. 19:3179-3191.[CrossRef][Medline]
    125. 125
  125. Moy, F. J., E. Glasfeld, L. Mosyak, and R. Powers. 2000. Solution structure of ZipA, a crucial component of Escherichia coli cell division. Biochemistry 39:9146-9156.[CrossRef][Medline]
    126. 126
  126. Mukherjee, A., and J. Lutkenhaus. 1994. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176:2754-2758.[Abstract/Free Full Text]
    127. 127
  127. Mukherjee, A., and J. Lutkenhaus. 1999. Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J. Bacteriol. 181:823-832.[Abstract/Free Full Text]
    128. 128
  128. Mukherjee, A., C. Saez, and J. Lutkenhaus. 2001. Assembly of an FtsZ mutant deficient in GTPase activity has implications for FtsZ assembly and the role of the Z ring in cell division. J. Bacteriol. 183:7190-7197.[Abstract/Free Full Text]
    129. 129
  129. Mulder, E., and C. L. Woldringh. 1989. Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA. J. Bacteriol. 171:4303-4314.[Abstract/Free Full Text]
    130. 130
  130. Nanninga, N. 1991. Cell division and peptidoglycan assembly in Escherichia coli. Mol. Microbiol. 5:791-795.[CrossRef][Medline]
    131. 131
  131. Nogales, E., K. H. Downing, L. A. Amos, and J. Löwe. 1998. Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5:451-458.[CrossRef][Medline]
    132. 132
  132. Nogales, E., M. Whittaker, R. A. Milligan, and K. H. Downing. 1999. High-resolution model of the microtubule. Cell 96:79-88.[CrossRef][Medline]
    133. 133
  133. Nogales, E., S. G. Wolf, and K. H. Downing. 1998. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391:199-203.[CrossRef][Medline]
    134. 134
  134. Ohashi, T., C. A. Hale, P. A. de Boer, and H. P. Erickson. 2002. Structural evidence that the P/Q domain of ZipA is an unstructured, flexible tether between the membrane and the C-terminal FtsZ-binding domain. J. Bacteriol. 184:4313-4315.[Abstract/Free Full Text]
    135. 135
  135. Pares, S., N. Mouz, Y. Petillot, R. Hakenbeck, and O. Dideberg. 1996. X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme. Nat. Struct. Biol. 3:284-289.[CrossRef][Medline]
    136. 136
  136. Pedersen, L. B., E. R. Angert, and P. Setlow. 1999. Septal localization of penicillin-binding protein 1 in Bacillus subtilis. J. Bacteriol. 181:3201-3211.[Abstract/Free Full Text]
    137. 137
  137. Pichoff, S., and J. Lutkenhaus. 2001. Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J. Bacteriol. 183:6630-6635.[Abstract/Free Full Text]
    138. 138
  138. Pichoff, S., and J. Lutkenhaus. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21:685-693.[CrossRef][Medline]
    139. 139
  139. Pichoff, S., B. Vollrath, C. Touriol, and J-P. Bouché. 1995. Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli. Mol. Microbiol. 18:321-329.[CrossRef][Medline]
    140. 140
  140. Pogliano, J., K. Pogliano, D. S. Weiss, R. Losick, and J. Beckwith. 1997. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc. Natl. Acad. Sci. USA 94:559-564.[Abstract/Free Full Text]
    141. 141
  141. Popham, D. L., and P. Setlow. 1996. Phenotypes of Bacillus subtilis mutants lacking multiple class a high-molecular-weight penicillin-binding proteins. J. Bacteriol. 178:2079-2085.[Abstract/Free Full Text]
    142. 142
  142. Raskin, D. M., and P. A. J. De Boer. 1999. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181:6419-6424.[Abstract/Free Full Text]
    143. 143
  143. Raskin, D. M., and P. A. J. De Boer. 1999. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 4971-4976.[Abstract/Free Full Text]
    144. 144
  144. RayChaudhuri, D. 1999. ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18:2372-2383.[CrossRef][Medline]
    145. 145
  145. Regamy, A., E. J. Harry, and R. G. Wake. 2000. Mid-cell Z ring assembly in the absence of entry into the elongation phase of the round of replication in bacteria: co-ordinating chromosome replication with cell division. Mol. Microbiol. 38:423-434.[CrossRef][Medline]
    146. 146
  146. Rothfield, L., S. Justice, and J. Garcia-Lara. 1999. Bacterial cell division. Annu. Rev. Genet. 33:423-448.[CrossRef][Medline]
    147. 147
  147. Rowland, S. L., V. L. Katis, S. R. Partridge, and R. G. Wake. 1997. DivIB, FtsZ and cell division in Bacillus subtilis. Mol. Microbiol. 23:295-302.[CrossRef][Medline]
    148. 148
  148. Sanchez, M., A. Valencia, M. J. Ferrandiz, C. Sander, and M. Vicente. 1994. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 13:4919-4925.[Medline]
    149. 149
  149. Scheffers, D., and A. J. Driessen. 2002. Immediate GTP hydrolysis upon FtsZ polymerization. Mol. Microbiol. 43:1517-1521.[CrossRef][Medline]
    150. 150
  150. Scheffers, D. J., J. G. de Wit, T. den Blaauwen, and A. J. Driessen. 2001. Substitution of a conserved aspartate allows cation-induced polymerization of FtsZ. FEBS Lett. 494:34-37.[CrossRef][Medline]
    151. 151
  151. Scheffers, D. J., J. G. de Wit, T. den Blaauwen, and A. J. M. Driessen. 2002. GTP hydrolysis of cell division protein FtsZ: evidence that the active site is formed by the association of monomers. Biochemistry 41:521-529.[CrossRef][Medline]
    152. 152
  152. Scheffers, D-J., T. den Blaauwen, and A. J. M. Driessen. 2000. Non-hydrolysable GTP-{gamma}-S stabilizes the FtsZ polymer in a GDP-bound state. Mol. Microbiol. 35:1211-1219.[CrossRef][Medline]
    153. 153
  153. Sievers, J., and J. Errington. 2000. Analysis of the essential cell division gene ftsL of Bacillus subtilis by mutagenesis and heterologous complementation. J. Bacteriol. 182:5572-5579.[Abstract/Free Full Text]
    154. 154
  154. Sievers, J., and J. Errington. 2000. The Bacillus subtilis cell division protein FtsL localizes to sites of septation and interacts with DivIC. Mol. Microbiol. 36:846-855.[CrossRef][Medline]
    155. 155
  155. Spratt, B. G. 1975. Distinct penicillin-binding proteins involved in the division, elongation and shape of Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 72:2999-3003.[Abstract/Free Full Text]
    156. 156
  156. Spratt, B. G. 1977. Temperature-sensitive cell division mutants of Escherichia coli with thermolabile penicillin-binding proteins. J. Bacteriol. 131:293-305.[Abstract/Free Full Text]
    157. 157
  157. Stragier, P. 2000. A gene odyssey: exploring the genomes of endospore-forming bacteria, p. 519-525. In Bacillus subtilis and its relatives: from genes to cells. L. Sonenshein, R. Losick, and J. A. Hoch American Society for Microbiology, Washington, D. C.
    158. 158
  158. Stricker, J., P. Maddox, E. D. Salmon, and H. P. Erickson. 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA 99:3171-3175.[Abstract/Free Full Text]
    159. 159
  159. Sun, Q., and W. Margolin. 1998. FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180:2050-2056.[Abstract/Free Full Text]
    160. 160
  160. Sun, Q., X-C. Yu, and W. Margolin. 1998. Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol. Microbiol. 29:491-503.[CrossRef][Medline]
    161. 161
  161. Szeto, T. H., S. L. Rowland, and G. F. King. 2001. The dimerization function of MinC resides in a structurally autonomous C-terminal domain. J. Bacteriol. 183:6684-6687.[Abstract/Free Full Text]
    162. 162
  162. Tamaki, S., H. Matsuzawa, and M. Matsuhashi. 1980. Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli. J. Bacteriol. 141:52-57.[Abstract/Free Full Text]
    163. 163
  163. Ueki, M., M. Wachi, H. K. Jung, F. Ishino, and M. Matsuhashi. 1992. Escherichia coli mraR gene involved in cell growth and division. J. Bacteriol. 174:7841-7843.[Abstract/Free Full Text]
    164. 164
  164. van den Ent F., L. Amos, and J. Löwe. 2001. Bacterial ancestry of actin and tubulin. Curr. Opin. Microbiol. 4:634-638.[CrossRef][Medline]
    165. 165
  165. van den Ent, F., and J. Löwe. 2000. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19:5300-5307.[CrossRef][Medline]
    166. 166
  166. Wang, L., M. K. Khattar, W. D. Donachie, and J. Lutkenhaus. 1998. FtsI and FtsW are localized to the septum in Escherichia coli. J. Bacteriol. 180:2810-2816.[Abstract/Free Full Text]
    167. 167
  167. Wang, L., and J. Lutkenhaus. 1998. FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol. Microbiol. 29:731-740.[CrossRef][Medline]
    168. 168
  168. Wang, X., and J. Lutkenhaus. 1993. The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration. Mol. Microbiol. 9:435-442.[CrossRef][Medline]
    169. 169
  169. Ward, J. E., Jr., and J. Lutkenhaus. 1985. Overproduction of FtsZ induces minicell formation in E. coli. Cell 42:941-949.[CrossRef][Medline]
    170. 170
  170. Weiss D. S., J. C. Chen, J-M. Ghigo, D. Boyd, and J. Beckwith. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J. Bacteriol. 181:508-520.[Abstract/Free Full Text]
    171. 171
  171. Weiss, D. S., K. Pogliano, M. Carson, L-M, Guzman, C. Fraipont, M. Nguyen-Distèche, R. Losick, and J. Beckwith. 1997. Localization of the Escherichia coli cell division protein FtsI (PBP3) to the division site and cell pole. Mol. Microbiol. 25:671-681.[CrossRef][Medline]
    172. 172
  172. Woldringh, C. L., E. Mulder, J. A. Valkenburg, F. B. Wientjes, A. Zaritsky, and N. Nanninga. 1990. Role of the nucleoid in the toporegulation of division. Res. Microbiol. 141:39-49.[CrossRef][Medline]
    173. 173
  173. Wu, L. J., A. H. Franks, and R. G. Wake. 1995. Replication through the terminus region of the Bacillus subtilis chromosome is not essential for the formation of a division septum that partitions the DNA. J. Bacteriol. 177:5711-5715.[Abstract/Free Full Text]
    174. 174
  174. Yan, K., K. H. Pearce, and D. J. Payne. 2000. A conserved residue at the extreme C-terminus of FtsZ is critical for the FtsA-FtsZ interaction in Staphylococcus aureus. Biochem. Biophys. Res. Commun. 270:387-392.[CrossRef][Medline]
    175. 175
  175. Yanouri, A., R. A. Daniel, J. Errington, and C. E. Buchanan. 1993. Cloning and sequencing of the cell division gene pbpB, which encodes penicillin-binding protein 2B in Bacillus subtilis. J. Bacteriol. 175:7604-7616.[Abstract/Free Full Text]
    176. 176
  176. Yu, X-C., A. H. Tran, Q. Sun, and W. Margolin. 1998. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180:1296-1304.[Abstract/Free Full Text]
    177. 177
  177. Zhang, Y., S. Rowland, G. King, E. Braswell, and L. Rothfield. 1998. The relationship between hetero-oligomer formation and function of the topological specificity domain of the Escherichia coli MinE protein. Mol. Microbiol. 30:265-273.[CrossRef][Medline]
    178. 178
  178. Zhao, C-R, P. A. J. De Boer, and L. I. Rothfield. 1995. Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc. Natl. Acad. Sci. USA 92:4313-4317.[Abstract/Free Full Text]

Microbiology and Molecular Biology Reviews, March 2003, p. 52-65, Vol. 67, No. 1
1092-2172/03/$08.00+0     DOI: 10.1128/MMBR.67.1.52-65.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Gerding, M. A., Liu, B., Bendezu, F. O., Hale, C. A., Bernhardt, T. G., de Boer, P. A. J. (2009). Self-Enhanced Accumulation of FtsN at Division Sites and Roles for Other Proteins with a SPOR Domain (DamX, DedD, and RlpA) in Escherichia coli Cell Constriction. J. Bacteriol. 191: 7383-7401 [Abstract] [Full Text]  
  • Masson, S., Kern, T., Le Gouellec, A., Giustini, C., Simorre, J.-P., Callow, P., Vernet, T., Gabel, F., Zapun, A. (2009). Central Domain of DivIB Caps the C-terminal Regions of the FtsL/DivIC Coiled-coil Rod. J. Biol. Chem. 284: 27687-27700 [Abstract] [Full Text]  
  • Marbouty, M., Saguez, C., Cassier-Chauvat, C., Chauvat, F. (2009). Characterization of the FtsZ-Interacting Septal Proteins SepF and Ftn6 in the Spherical-Celled Cyanobacterium Synechocystis Strain PCC 6803. J. Bacteriol. 191: 6178-6185 [Abstract] [Full Text]  
  • Xu, Q., Traag, B. A., Willemse, J., McMullan, D., Miller, M. D., Elsliger, M.-A., Abdubek, P., Astakhova, T., Axelrod, H. L., Bakolitsa, C., Carlton, D., Chen, C., Chiu, H.-J., Chruszcz, M., Clayton, T., Das, D., Deller, M. C., Duan, L., Ellrott, K., Ernst, D., Farr, C. L., Feuerhelm, J., Grant, J. C., Grzechnik, A., Grzechnik, S. K., Han, G. W., Jaroszewski, L., Jin, K. K., Klock, H. E., Knuth, M. W., Kozbial, P., Krishna, S. S., Kumar, A., Marciano, D., Minor, W., Mommaas, A. M., Morse, A. T., Nigoghossian, E., Nopakun, A., Okach, L., Oommachen, S., Paulsen, J., Puckett, C., Reyes, R., Rife, C. L., Sefcovic, N., Tien, H. J., Trame, C. B., van den Bedem, H., Wang, S., Weekes, D., Hodgson, K. O., Wooley, J., Deacon, A. M., Godzik, A., Lesley, S. A., Wilson, I. A., van Wezel, G. P. (2009). Structural and Functional Characterizations of SsgB, a Conserved Activator of Developmental Cell Division in Morphologically Complex Actinomycetes. J. Biol. Chem. 284: 25268-25279 [Abstract] [Full Text]  
  • Marbouty, M., Mazouni, K., Saguez, C., Cassier-Chauvat, C., Chauvat, F. (2009). Characterization of the Synechocystis Strain PCC 6803 Penicillin-Binding Proteins and Cytokinetic Proteins FtsQ and FtsW and Their Network of Interactions with ZipN. J. Bacteriol. 191: 5123-5133 [Abstract] [Full Text]  
  • Gamba, P., Veening, J.-W., Saunders, N. J., Hamoen, L. W., Daniel, R. A. (2009). Two-Step Assembly Dynamics of the Bacillus subtilis Divisome. J. Bacteriol. 191: 4186-4194 [Abstract] [Full Text]  
  • Slayden, R. A., Belisle, J. T. (2009). Morphological features and signature gene response elicited by inactivation of FtsI in Mycobacterium tuberculosis. J Antimicrob Chemother 63: 451-457 [Abstract] [Full Text]  
  • Gregory, J. A., Becker, E. C., Pogliano, K. (2008). Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev. 22: 3475-3488 [Abstract] [Full Text]  
  • Tavares, J. R., de Souza, R. F., Meira, G. L. S., Gueiros-Filho, F. J. (2008). Cytological Characterization of YpsB, a Novel Component of the Bacillus subtilis Divisome. J. Bacteriol. 190: 7096-7107 [Abstract] [Full Text]  
  • Maggi, S., Massidda, O., Luzi, G., Fadda, D., Paolozzi, L., Ghelardini, P. (2008). Division protein interaction web: identification of a phylogenetically conserved common interactome between Streptococcus pneumoniae and Escherichia coli. Microbiology 154: 3042-3052 [Abstract] [Full Text]  
  • Bible, A. N., Stephens, B. B., Ortega, D. R., Xie, Z., Alexandre, G. (2008). Function of a Chemotaxis-Like Signal Transduction Pathway in Modulating Motility, Cell Clumping, and Cell Length in the Alphaproteobacterium Azospirillum brasilense. J. Bacteriol. 190: 6365-6375 [Abstract] [Full Text]  
  • Haydon, D. J., Stokes, N. R., Ure, R., Galbraith, G., Bennett, J. M., Brown, D. R., Baker, P. J., Barynin, V. V., Rice, D. W., Sedelnikova, S. E., Heal, J. R., Sheridan, J. M., Aiwale, S. T., Chauhan, P. K., Srivastava, A., Taneja, A., Collins, I., Errington, J., Czaplewski, L. G. (2008). An Inhibitor of FtsZ with Potent and Selective Anti-Staphylococcal Activity. Science 321: 1673-1675 [Abstract] [Full Text]  
  • Robichon, C., King, G. F., Goehring, N. W., Beckwith, J. (2008). Artificial Septal Targeting of Bacillus subtilis Cell Division Proteins in Escherichia coli: an Interspecies Approach to the Study of Protein-Protein Interactions in Multiprotein Complexes. J. Bacteriol. 190: 6048-6059 [Abstract] [Full Text]  
  • Mistry, B. V., Del Sol, R., Wright, C., Findlay, K., Dyson, P. (2008). FtsW Is a Dispensable Cell Division Protein Required for Z-Ring Stabilization during Sporulation Septation in Streptomyces coelicolor. J. Bacteriol. 190: 5555-5566 [Abstract] [Full Text]  
  • Le Gouellec, A., Roux, L., Fadda, D., Massidda, O., Vernet, T., Zapun, A. (2008). Roles of Pneumococcal DivIB in Cell Division. J. Bacteriol. 190: 4501-4511 [Abstract] [Full Text]  
  • Srinivasan, R., Mishra, M., Wu, L., Yin, Z., Balasubramanian, M. K. (2008). The bacterial cell division protein FtsZ assembles into cytoplasmic rings in fission yeast. Genes Dev. 22: 1741-1746 [Abstract] [Full Text]  
  • Dajkovic, A., Mukherjee, A., Lutkenhaus, J. (2008). Investigation of Regulation of FtsZ Assembly by SulA and Development of a Model for FtsZ Polymerization. J. Bacteriol. 190: 2513-2526 [Abstract] [Full Text]  
  • Hett, E. C., Rubin, E. J. (2008). Bacterial Growth and Cell Division: a Mycobacterial Perspective. Microbiol. Mol. Biol. Rev. 72: 126-156 [Abstract] [Full Text]  
  • Campo, N., Marquis, K. A., Rudner, D. Z. (2008). SpoIIQ Anchors Membrane Proteins on Both Sides of the Sporulation Septum in Bacillus subtilis. J. Biol. Chem. 283: 4975-4982 [Abstract] [Full Text]  
  • Meredith, D. H., Plank, M., Lewis, P. J. (2008). Different patterns of integral membrane protein localization during cell division in Bacillus subtilis. Microbiology 154: 64-71 [Abstract] [Full Text]  
  • Haeusser, D. P., Garza, A. C., Buscher, A. Z., Levin, P. A. (2007). The Division Inhibitor EzrA Contains a Seven-Residue Patch Required for Maintaining the Dynamic Nature of the Medial FtsZ Ring. J. Bacteriol. 189: 9001-9010 [Abstract] [Full Text]  
  • Rosario, C. J., Singer, M. (2007). The Myxococcus xanthus Developmental Program Can Be Delayed by Inhibition of DNA Replication. J. Bacteriol. 189: 8793-8800 [Abstract] [Full Text]  
  • Bennett, J. A., Aimino, R. M., McCormick, J. R. (2007). Streptomyces coelicolor Genes ftsL and divIC Play a Role in Cell Division but Are Dispensable for Colony Formation. J. Bacteriol. 189: 8982-8992 [Abstract] [Full Text]  
  • van Heijenoort, J. (2007). Lipid Intermediates in the Biosynthesis of Bacterial Peptidoglycan. Microbiol. Mol. Biol. Rev. 71: 620-635 [Abstract] [Full Text]  
  • Samaluru, H., SaiSree, L., Reddy, M. (2007). Role of SufI (FtsP) in Cell Division of Escherichia coli: Evidence for Its Involvement in Stabilizing the Assembly of the Divisome. J. Bacteriol. 189: 8044-8052 [Abstract] [Full Text]  
  • Russell, J. H., Keiler, K. C. (2007). Peptide Signals Encode Protein Localization. J. Bacteriol. 189: 7581-7585 [Abstract] [Full Text]  
  • Lan, G., Wolgemuth, C. W., Sun, S. X. (2007). Z-ring force and cell shape during division in rod-like bacteria. Proc. Natl. Acad. Sci. USA 104: 16110-16115 [Abstract] [Full Text]  
  • Lu, Z., Takeuchi, M., Sato, T. (2007). The LysR-Type Transcriptional Regulator YofA Controls Cell Division through the Regulation of Expression of ftsW in Bacillus subtilis. J. Bacteriol. 189: 5642-5651 [Abstract] [Full Text]  
  • Bogush, M., Xenopoulos, P., Piggot, P. J. (2007). Separation of Chromosome Termini during Sporulation of Bacillus subtilis Depends on SpoIIIE. J. Bacteriol. 189: 3564-3572 [Abstract] [Full Text]  
  • Watt, R. M., Wang, J., Leong, M., Kung, H.-f., Cheah, K. S.E., Liu, D., Danchin, A., Huang, J.-D. (2007). Visualizing the proteome of Escherichia coli: an efficient and versatile method for labeling chromosomal coding DNA sequences (CDSs) with fluorescent protein genes. Nucleic Acids Res 35: e37-e37 [Abstract] [Full Text]  
  • Norris, V., den Blaauwen, T., Cabin-Flaman, A., Doi, R. H., Harshey, R., Janniere, L., Jimenez-Sanchez, A., Jin, D. J., Levin, P. A., Mileykovskaya, E., Minsky, A., Saier, M. Jr., Skarstad, K. (2007). Functional Taxonomy of Bacterial Hyperstructures. Microbiol. Mol. Biol. Rev. 71: 230-253 [Abstract] [Full Text]  
  • Van La, M., Barbry, P., Raoult, D., Renesto, P. (2007). Molecular basis of Tropheryma whipplei doxycycline susceptibility examined by transcriptional profiling. J Antimicrob Chemother 59: 370-377 [Abstract] [Full Text]  
  • Fadda, D., Santona, A., D'Ulisse, V., Ghelardini, P., Ennas, M. G., Whalen, M. B., Massidda, O. (2007). Streptococcus pneumoniae DivIVA: Localization and Interactions in a MinCD-Free Context. J. Bacteriol. 189: 1288-1298 [Abstract] [Full Text]  
  • Cheng, J., Sibley, C. D., Zaheer, R., Finan, T. M. (2007). A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology 153: 375-387 [Abstract] [Full Text]  
  • D'Ulisse, V., Fagioli, M., Ghelardini, P., Paolozzi, L. (2007). Three functional subdomains of the Escherichia coli FtsQ protein are involved in its interaction with the other division proteins. Microbiology 153: 124-138 [Abstract] [Full Text]  
  • Reddy, M. (2007). Role of FtsEX in Cell Division of Escherichia coli: Viability of ftsEX Mutants Is Dependent on Functional SufI or High Osmotic Strength. J. Bacteriol. 189: 98-108 [Abstract] [Full Text]  
  • Tracz, D. M., Backhouse, P. G., Olson, A. B., McCrea, J. K., Walsh, J. A., Ng, L.-K., Gilmour, M. W. (2007). Rapid detection of Vibrio species using liquid microsphere arrays and real-time PCR targeting the ftsZ locus. J Med Microbiol 56: 56-65 [Abstract] [Full Text]  
  • Thakur, M., Chakraborti, P. K. (2006). GTPase Activity of Mycobacterial FtsZ Is Impaired Due to Its Transphosphorylation by the Eukaryotic-type Ser/Thr Kinase, PknA. J. Biol. Chem. 281: 40107-40113 [Abstract] [Full Text]  
  • Carballido-Lopez, R. (2006). The Bacterial Actin-Like Cytoskeleton. Microbiol. Mol. Biol. Rev. 70: 888-909 [Abstract] [Full Text]  
  • Watters, C. (2006). The Bacterial Cytoskeleton. cellbioed 5: 306-310 [Full Text]  
  • Thompson, L. S., Beech, P. L., Real, G., Henriques, A. O., Harry, E. J. (2006). Requirement for the Cell Division Protein DivIB in Polar Cell Division and Engulfment during Sporulation in Bacillus subtilis. J. Bacteriol. 188: 7677-7685 [Abstract] [Full Text]  
  • Daniel, R. A., Noirot-Gros, M.-F., Noirot, P., Errington, J. (2006). Multiple Interactions between the Transmembrane Division Proteins of Bacillus subtilis and the Role of FtsL Instability in Divisome Assembly. J. Bacteriol. 188: 7396-7404 [Abstract] [Full Text]  
  • Osawa, M., Erickson, H. P. (2006). FtsZ from Divergent Foreign Bacteria Can Function for Cell Division in Escherichia coli.. J. Bacteriol. 188: 7132-7140 [Abstract] [Full Text]  
  • Young, K. D. (2006). The Selective Value of Bacterial Shape. Microbiol. Mol. Biol. Rev. 70: 660-703 [Abstract] [Full Text]  
  • Shih, Y.-L., Rothfield, L. (2006). The Bacterial Cytoskeleton. Microbiol. Mol. Biol. Rev. 70: 729-754 [Abstract] [Full Text]  
  • Leimanis, S., Hoyez, N., Hubert, S., Laschet, M., Sauvage, E., Brasseur, R., Coyette, J. (2006). PBP5 Complementation of a PBP3 Deficiency in Enterococcus hirae.. J. Bacteriol. 188: 6298-6307 [Abstract] [Full Text]  
  • Lambden, P. R., Pickett, M. A., Clarke, I. N. (2006). The effect of penicillin on Chlamydia trachomatis DNA replication.. Microbiology 152: 2573-2578 [Abstract] [Full Text]  
  • Sakr, S., Thyssen, M., Denis, M., Zhang, C.-C. (2006). Relationship among Several Key Cell Cycle Events in the Developmental Cyanobacterium Anabaena sp. Strain PCC 7120.. J. Bacteriol. 188: 5958-5965 [Abstract] [Full Text]  
  • Robson, S. A., King, G. F. (2006). Domain architecture and structure of the bacterial cell division protein DivIB. Proc. Natl. Acad. Sci. USA 103: 6700-6705 [Abstract] [Full Text]  
  • Kawai, Y., Ogasawara, N. (2006). Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division.. Microbiology 152: 1129-1141 [Abstract] [Full Text]  
  • Sakr, S., Jeanjean, R., Zhang, C.-C., Arcondeguy, T. (2006). Inhibition of Cell Division Suppresses Heterocyst Development in Anabaena sp. Strain PCC 7120. J. Bacteriol. 188: 1396-1404 [Abstract] [Full Text]  
  • Del Sol, R., Mullins, J. G. L., Grantcharova, N., Flardh, K., Dyson, P. (2006). Influence of CrgA on Assembly of the Cell Division Protein FtsZ during Development of Streptomyces coelicolor. J. Bacteriol. 188: 1540-1550 [Abstract] [Full Text]  
  • Chatterjee, S. S., Hossain, H., Otten, S., Kuenne, C., Kuchmina, K., Machata, S., Domann, E., Chakraborty, T., Hain, T. (2006). Intracellular Gene Expression Profile of Listeria monocytogenes. Infect. Immun. 74: 1323-1338 [Abstract] [Full Text]  
  • Vicente, M., Rico, A. I., Martinez-Arteaga, R., Mingorance, J. (2006). Septum Enlightenment: Assembly of Bacterial Division Proteins. J. Bacteriol. 188: 19-27 [Full Text]  
  • Dye, N. A., Pincus, Z., Theriot, J. A., Shapiro, L., Gitai, Z. (2005). Two independent spiral structures control cell shape in Caulobacter. Proc. Natl. Acad. Sci. USA 102: 18608-18613 [Abstract] [Full Text]  
  • Wang, Y., Xu, X. (2005). Regulation by hetC of Genes Required for Heterocyst Differentiation and Cell Division in Anabaena sp. Strain PCC 7120. J. Bacteriol. 187: 8489-8493 [Abstract] [Full Text]  
  • Stokes, N. R., Sievers, J., Barker, S., Bennett, J. M., Brown, D. R., Collins, I., Errington, V. M., Foulger, D., Hall, M., Halsey, R., Johnson, H., Rose, V., Thomaides, H. B., Haydon, D. J., Czaplewski, L. G., Errington, J. (2005). Novel Inhibitors of Bacterial Cytokinesis Identified by a Cell-based Antibiotic Screening Assay. J. Biol. Chem. 280: 39709-39715 [Abstract] [Full Text]  
  • Harold, F. M. (2005). Molecules into Cells: Specifying Spatial Architecture. Microbiol. Mol. Biol. Rev. 69: 544-564 [Abstract] [Full Text]  
  • Scheffers, D.-J., Pinho, M. G. (2005). Bacterial Cell Wall Synthesis: New Insights from Localization Studies. Microbiol. Mol. Biol. Rev. 69: 585-607 [Abstract] [Full Text]  
  • Lau, S. Y., Zgurskaya, H. I. (2005). Cell Division Defects in Escherichia coli Deficient in the Multidrug Efflux Transporter AcrEF-TolC. J. Bacteriol. 187: 7815-7825 [Abstract] [Full Text]  
  • Judd, E. M., Comolli, L. R., Chen, J. C., Downing, K. H., Moerner, W. E., McAdams, H. H. (2005). Distinct Constrictive Processes, Separated in Time and Space, Divide Caulobacter Inner and Outer Membranes. J. Bacteriol. 187: 6874-6882 [Abstract] [Full Text]  
  • Jensen, S. O., Thompson, L. S., Harry, E. J. (2005). Cell Division in Bacillus subtilis: FtsZ and FtsA Association Is Z-Ring Independent, and FtsA Is Required for Efficient Midcell Z-Ring Assembly. J. Bacteriol. 187: 6536-6544 [Abstract] [Full Text]  
  • Nilsen, T., Yan, A. W., Gale, G., Goldberg, M. B. (2005). Presence of Multiple Sites Containing Polar Material in Spherical Escherichia coli Cells That Lack MreB. J. Bacteriol. 187: 6187-6196 [Abstract] [Full Text]  
  • Feucht, A., Errington, J. (2005). ftsZ mutations affecting cell division frequency, placement and morphology in Bacillus subtilis. Microbiology 151: 2053-2064 [Abstract] [Full Text]  
  • Carniol, K., Ben-Yehuda, S., King, N., Losick, R. (2005). Genetic Dissection of the Sporulation Protein SpoIIE and Its Role in Asymmetric Division in Bacillus subtilis. J. Bacteriol. 187: 3511-3520 [Abstract] [Full Text]  
  • Grantcharova, N., Lustig, U., Flardh, K. (2005). Dynamics of FtsZ Assembly during Sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 187: 3227-3237 [Abstract] [Full Text]  
  • Strauss, B., Kelly, K., Ekiert, D. (2005). Cytochrome Oxidase Deficiency Protects Escherichia coli from Cell Death but Not from Filamentation Due to Thymine Deficiency or DNA Polymerase Inactivation. J. Bacteriol. 187: 2827-2835 [Abstract] [Full Text]  
  • Nishibori, A., Kusaka, J., Hara, H., Umeda, M., Matsumoto, K. (2005). Phosphatidylethanolamine Domains and Localization of Phospholipid Synthases in Bacillus subtilis Membranes. J. Bacteriol. 187: 2163-2174 [Abstract] [Full Text]  
  • Scheffers, D.-J. (2005). Dynamic localization of penicillin-binding proteins during spore development in Bacillus subtilis. Microbiology 151: 999-1012 [Abstract] [Full Text]  
  • Ehrt, S., Guo, X. V., Hickey, C. M., Ryou, M., Monteleone, M., Riley, L. W., Schnappinger, D. (2005). Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res 33: e21-e21 [Abstract] [Full Text]  
  • Paradis-Bleau, C., Sanschagrin, F., Levesque, R. C. (2005). Peptide inhibitors of the essential cell division protein FtsA. Protein Eng Des Sel 18: 85-91 [Abstract] [Full Text]  
  • Macheboeuf, P., Di Guilmi, A. M., Job, V., Vernet, T., Dideberg, O., Dessen, A. (2005). Active site restructuring regulates ligand recognition in class A penicillin-binding proteins. Proc. Natl. Acad. Sci. USA 102: 577-582 [Abstract] [Full Text]  
  • Wagner, J. K., Galvani, C. D., Brun, Y. V. (2005). Caulobacter crescentus Requires RodA and MreB for Stalk Synthesis and Prevention of Ectopic Pole Formation. J. Bacteriol. 187: 544-553 [Abstract] [Full Text]  
  • Slovak, P. M., Wadhams, G. H., Armitage, J. P. (2005). Localization of MreB in Rhodobacter sphaeroides under Conditions Causing Changes in Cell Shape and Membrane Structure. J. Bacteriol. 187: 54-64 [Abstract] [Full Text]  
  • Wissel, M. C., Wendt, J. L., Mitchell, C. J., Weiss, D. S. (2005). The Transmembrane Helix of the Escherichia coli Division Protein FtsI Localizes to the Septal Ring. J. Bacteriol. 187: 320-328 [Abstract] [Full Text]  
  • Goehring, N. W., Gueiros-Filho, F., Beckwith, J. (2005). Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. Genes Dev. 19: 127-137 [Abstract] [Full Text]  
  • Pastoret, S., Fraipont, C., den Blaauwen, T., Wolf, B., Aarsman, M. E. G., Piette, A., Thomas, A., Brasseur, R., Nguyen-Disteche, M. (2004). Functional Analysis of the Cell Division Protein FtsW of Escherichia coli. J. Bacteriol. 186: 8370-8379 [Abstract] [Full Text]  
  • Blaylock, B., Jiang, X., Rubio, A., Moran, C. P. Jr., Pogliano, K. (2004). Zipper-like interaction between proteins in adjacent daughter cells mediates protein localization. Genes Dev. 18: 2916-2928 [Abstract] [Full Text]  
  • O'Reilly, E. K., Kreuzer, K. N. (2004). Isolation of SOS Constitutive Mutants of Escherichia coli. J. Bacteriol. 186: 7149-7160 [Abstract] [Full Text]  
  • Szeto, J., Acharya, S., Eng, N. F., Dillon, J.-A. R. (2004). The N Terminus of MinD Contains Determinants Which Affect Its Dynamic Localization and Enzymatic Activity. J. Bacteriol. 186: 7175-7185 [Abstract] [Full Text]  
  • Iyer, L. M., Makarova, K. S., Koonin, E. V., Aravind, L. (2004). Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32: 5260-5279 [Abstract] [Full Text]  
  • Piette, A., Fraipont, C., den Blaauwen, T., Aarsman, M. E. G., Pastoret, S., Nguyen-Disteche, M. (2004). Structural Determinants Required To Target Penicillin-Binding Protein 3 to the Septum of Escherichia coli. J. Bacteriol. 186: 6110-6117 [Abstract] [Full Text]  
  • Anderson, D. E., Gueiros-Filho, F. J., Erickson, H. P. (2004). Assembly Dynamics of FtsZ Rings in Bacillus subtilis and Escherichia coli and Effects of FtsZ-Regulating Proteins. J. Bacteriol. 186: 5775-5781 [Abstract] [Full Text]  
  • Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T., Takamiya, K.-i. (2004). ARC3, a Chloroplast Division Factor, is a Chimera of Prokaryotic FtsZ and Part of Eukaryotic Phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45: 960-967 [Abstract] [Full Text]  
  • Scheffers, D.-J., Errington, J. (2004). PBP1 Is a Component of the Bacillus subtilis Cell Division Machinery. J. Bacteriol. 186: 5153-5156 [Abstract] [Full Text]  
  • Santra, M. K., Beuria, T. K., Banerjee, A., Panda, D. (2004). Ruthenium Red-induced Bundling of Bacterial Cell Division Protein, FtsZ. J. Biol. Chem. 279: 25959-25965 [Abstract] [Full Text]  
  • Gitai, Z., Dye, N., Shapiro, L. (2004). From the Cover: An actin-like gene can determine cell polarity in bacteria. Proc. Natl. Acad. Sci. USA 101: 8643-8648 [Abstract] [Full Text]  
  • Hilbert, D. W., Piggot, P. J. (2004). Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation. Microbiol. Mol. Biol. Rev. 68: 234-262 [Abstract] [Full Text]  
  • Rocha, E. P. C. (2004). The replication-related organization of bacterial genomes. Microbiology 150: 1609-1627 [Abstract] [Full Text]  
  • Johnson, J. E., Lackner, L. L., Hale, C. A., de Boer, P. A. J. (2004). ZipA Is Required for Targeting of DMinC/DicB, but Not DMinC/MinD, Complexes to Septal Ring Assemblies in Escherichia coli. J. Bacteriol. 186: 2418-2429 [Abstract] [Full Text]  
  • Strauss, B., Kelly, K., Dincman, T., Ekiert, D., Biesieda, T., Song, R. (2004). Cell Death in Escherichia coli dnaE(Ts) Mutants Incubated at a Nonpermissive Temperature Is Prevented by Mutation in the cydA Gene. J. Bacteriol. 186: 2147-2155 [Abstract] [Full Text]  
  • Wikstrom, M., Xie, J., Bogdanov, M., Mileykovskaya, E., Heacock, P., Wieslander, A., Dowhan, W. (2004). Monoglucosyldiacylglycerol, a Foreign Lipid, Can Substitute for Phosphatidylethanolamine in Essential Membrane-associated Functions in Escherichia coli. J. Biol. Chem. 279: 10484-10493 [Abstract] [Full Text]  
  • Schmidt, K. L., Peterson, N. D., Kustusch, R. J., Wissel, M. C., Graham, B., Phillips, G. J., Weiss, D. S. (2004). A Predicted ABC Transporter, FtsEX, Is Needed for Cell Division in Escherichia coli. J. Bacteriol. 186: 785-793 [Abstract] [Full Text]  
  • Arends, S. J. R., Weiss, D. S. (2004). Inhibiting Cell Division in Escherichia coli Has Little If Any Effect on Gene Expression. J. Bacteriol. 186: 880-884 [Abstract] [Full Text]  
  • Janakiraman, A., Goldberg, M. B. (2004). From the Cover: Evidence for polar positional information independent of cell division and nucleoid occlusion. Proc. Natl. Acad. Sci. USA 101: 835-840 [Abstract] [Full Text]  
  • Wissel, M. C., Weiss, D. S. (2004). Genetic Analysis of the Cell Division Protein FtsI (PBP3): Amino Acid Substitutions That Impair Septal Localization of FtsI and Recruitment of FtsN. J. Bacteriol. 186: 490-502 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Errington, J.
Right arrow Articles by Scheffers, D.-J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Errington, J.
Right arrow Articles by Scheffers, D.-J.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»