Previous Article | Next Article 
Microbiology and Molecular Biology Reviews, March 2006, p. 192-221, Vol. 70, No. 1
1092-2172/06/$08.00+0 doi:10.1128/MMBR.70.1.192-221.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
Sortases and the Art of Anchoring Proteins to the Envelopes of Gram-Positive Bacteria
Luciano A. Marraffini,1
Andrea C. DeDent,2 and
Olaf Schneewind2*
Department of Microbiology,2
Department of Molecular Genetics and Cell Biology, University of Chicago, 920 East 58th Street, Chicago, Illinois 606371
The cell wall envelopes of gram-positive bacteria represent a surface organelle that not only functions as a cytoskeletal element but also promotes interactions between bacteria and their environment. Cell wall peptidoglycan is covalently and noncovalently decorated with teichoic acids, polysaccharides, and proteins. The sum of these molecular decorations provides bacterial envelopes with species- and strain-specific properties that are ultimately responsible for bacterial virulence, interactions with host immune systems, and the development of disease symptoms or successful outcomes of infections. Surface proteins typically carry two topogenic sequences, i.e., N-terminal signal peptides and C-terminal sorting signals. Sortases catalyze a transpeptidation reaction by first cleaving a surface protein substrate at the cell wall sorting signal. The resulting acyl enzyme intermediates between sortases and their substrates are then resolved by the nucleophilic attack of amino groups, typically provided by the cell wall cross bridges of peptidoglycan precursors. The surface protein linked to peptidoglycan is then incorporated into the envelope and displayed on the microbial surface. This review focuses on the mechanisms of surface protein anchoring to the cell wall envelope by sortases and the role that these enzymes play in bacterial physiology and pathogenesis.
* Corresponding author. Mailing address: Department of Microbiology, Genetics and Cell Biology, University of Chicago, 920 East 58th Street, Chicago, IL 60637. Phone: (773) 834-9060. Fax: (773) 834-8150. E-mail:
oschnee{at}bsd.uchicago.edu.
Microbiology and Molecular Biology Reviews, March 2006, p. 192-221, Vol. 70, No. 1
1092-2172/06/$08.00+0 doi:10.1128/MMBR.70.1.192-221.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Gianfaldoni, C., Maccari, S., Pancotto, L., Rossi, G., Hilleringmann, M., Pansegrau, W., Sinisi, A., Moschioni, M., Masignani, V., Rappuoli, R., Del Giudice, G., Ruggiero, P.
(2009). Sortase A Confers Protection against Streptococcus pneumoniae in Mice. Infect. Immun.
77: 2957-2961
[Abstract]
[Full Text]
-
Antos, J. M., Popp, M. W.-L., Ernst, R., Chew, G.-L., Spooner, E., Ploegh, H. L.
(2009). A Straight Path to Circular Proteins. J. Biol. Chem.
284: 16028-16036
[Abstract]
[Full Text]
-
Budzik, J. M., Oh, S.-Y., Schneewind, O.
(2009). Sortase D Forms the Covalent Bond That Links BcpB to the Tip of Bacillus cereus Pili. J. Biol. Chem.
284: 12989-12997
[Abstract]
[Full Text]
-
Bryan, J. D., Shelver, D. W.
(2009). Streptococcus agalactiae CspA Is a Serine Protease That Inactivates Chemokines. J. Bacteriol.
191: 1847-1854
[Abstract]
[Full Text]
-
Mariscotti, J. F., Portillo, F. G.-d., Pucciarelli, M. G.
(2009). The Listeria monocytogenes Sortase-B Recognizes Varied Amino Acids at Position 2 of the Sorting Motif. J. Biol. Chem.
284: 6140-6146
[Abstract]
[Full Text]
-
Budzik, J. M., Oh, S.-Y., Schneewind, O.
(2008). Cell Wall Anchor Structure of BcpA Pili in Bacillus anthracis. J. Biol. Chem.
283: 36676-36686
[Abstract]
[Full Text]
-
Raz, A., Fischetti, V. A.
(2008). Sortase A localizes to distinct foci on the Streptococcus pyogenes membrane. Proc. Natl. Acad. Sci. USA
105: 18549-18554
[Abstract]
[Full Text]
-
Fisher, M., Huang, Y.-S., Li, X., McIver, K. S., Toukoki, C., Eichenbaum, Z.
(2008). Shr Is a Broad-Spectrum Surface Receptor That Contributes to Adherence and Virulence in Group A Streptococcus. Infect. Immun.
76: 5006-5015
[Abstract]
[Full Text]
-
Wiens, G. D., Rockey, D. D., Wu, Z., Chang, J., Levy, R., Crane, S., Chen, D. S., Capri, G. R., Burnett, J. R., Sudheesh, P. S., Schipma, M. J., Burd, H., Bhattacharyya, A., Rhodes, L. D., Kaul, R., Strom, M. S.
(2008). Genome Sequence of the Fish Pathogen Renibacterium salmoninarum Suggests Reductive Evolution away from an Environmental Arthrobacter Ancestor. J. Bacteriol.
190: 6970-6982
[Abstract]
[Full Text]
-
Sillanpaa, J., Nallapareddy, S. R., Prakash, V. P., Qin, X., Hook, M., Weinstock, G. M., Murray, B. E.
(2008). Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium. Microbiology
154: 3199-3211
[Abstract]
[Full Text]
-
Mandlik, A., Das, A., Ton-That, H.
(2008). From the Cover: The molecular switch that activates the cell wall anchoring step of pilus assembly in gram-positive bacteria. Proc. Natl. Acad. Sci. USA
105: 14147-14152
[Abstract]
[Full Text]
-
Oh, S.-Y., Budzik, J. M., Schneewind, O.
(2008). Sortases make pili from three ingredients. Proc. Natl. Acad. Sci. USA
105: 13703-13704
[Full Text]
-
Adams, J. J., Gregg, K., Bayer, E. A., Boraston, A. B., Smith, S. P.
(2008). Structural basis of Clostridium perfringens toxin complex formation. Proc. Natl. Acad. Sci. USA
105: 12194-12199
[Abstract]
[Full Text]
-
Nobbs, A. H., Rosini, R., Rinaudo, C. D., Maione, D., Grandi, G., Telford, J. L.
(2008). Sortase A Utilizes an Ancillary Protein Anchor for Efficient Cell Wall Anchoring of Pili in Streptococcus agalactiae. Infect. Immun.
76: 3550-3560
[Abstract]
[Full Text]
-
Budzik, J. M., Marraffini, L. A., Souda, P., Whitelegge, J. P., Faull, K. F., Schneewind, O.
(2008). Amide bonds assemble pili on the surface of bacilli. Proc. Natl. Acad. Sci. USA
105: 10215-10220
[Abstract]
[Full Text]
-
Rosch, J. W., Vega, L. A., Beyer, J. M., Lin, A., Caparon, M. G.
(2008). The Signal Recognition Particle Pathway Is Required for Virulence in Streptococcus pyogenes. Infect. Immun.
76: 2612-2619
[Abstract]
[Full Text]
-
Bentley, M. L., Lamb, E. C., McCafferty, D. G.
(2008). Mutagenesis Studies of Substrate Recognition and Catalysis in the Sortase A Transpeptidase from Staphylococcus aureus. J. Biol. Chem.
283: 14762-14771
[Abstract]
[Full Text]
-
Lloyd, A. J., Gilbey, A. M., Blewett, A. M., De Pascale, G., El Zoeiby, A., Levesque, R. C., Catherwood, A. C., Tomasz, A., Bugg, T. D. H., Roper, D. I., Dowson, C. G.
(2008). Characterization of tRNA-dependent Peptide Bond Formation by MurM in the Synthesis of Streptococcus pneumoniae Peptidoglycan. J. Biol. Chem.
283: 6402-6417
[Abstract]
[Full Text]
-
Leibig, M., Krismer, B., Kolb, M., Friede, A., Gotz, F., Bertram, R.
(2008). Marker Removal in Staphylococci via Cre Recombinase and Different lox Sites. Appl. Environ. Microbiol.
74: 1316-1323
[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]
-
Kemp, K. D., Singh, K. V., Nallapareddy, S. R., Murray, B. E.
(2007). Relative Contributions of Enterococcus faecalis OG1RF Sortase-Encoding Genes, srtA and bps (srtC), to Biofilm Formation and a Murine Model of Urinary Tract Infection. Infect. Immun.
75: 5399-5404
[Abstract]
[Full Text]
-
Marraffini, L. A., Schneewind, O.
(2007). Sortase C-Mediated Anchoring of BasI to the Cell Wall Envelope of Bacillus anthracis. J. Bacteriol.
189: 6425-6436
[Abstract]
[Full Text]
-
Maresso, A. W., Wu, R., Kern, J. W., Zhang, R., Janik, D., Missiakas, D. M., Duban, M.-E., Joachimiak, A., Schneewind, O.
(2007). Activation of Inhibitors by Sortase Triggers Irreversible Modification of the Active Site. J. Biol. Chem.
282: 23129-23139
[Abstract]
[Full Text]
-
DeDent, A. C., McAdow, M., Schneewind, O.
(2007). Distribution of Protein A on the Surface of Staphylococcus aureus. J. Bacteriol.
189: 4473-4484
[Abstract]
[Full Text]
-
Bierne, H., Cossart, P.
(2007). Listeria monocytogenes Surface Proteins: from Genome Predictions to Function. Microbiol. Mol. Biol. Rev.
71: 377-397
[Abstract]
[Full Text]
-
Magnet, S., Bellais, S., Dubost, L., Fourgeaud, M., Mainardi, J.-L., Petit-Frere, S., Marie, A., Mengin-Lecreulx, D., Arthur, M., Gutmann, L.
(2007). Identification of the L,D-Transpeptidases Responsible for Attachment of the Braun Lipoprotein to Escherichia coli Peptidoglycan. J. Bacteriol.
189: 3927-3931
[Abstract]
[Full Text]
-
Nomellini, J. F., Duncan, G., Dorocicz, I. R., Smit, J.
(2007). S-Layer-Mediated Display of the Immunoglobulin G-Binding Domain of Streptococcal Protein G on the Surface of Caulobacter crescentus: Development of an Immunoactive Reagent. Appl. Environ. Microbiol.
73: 3245-3253
[Abstract]
[Full Text]
-
Mishra, A., Das, A., Cisar, J. O., Ton-That, H.
(2007). Sortase-Catalyzed Assembly of Distinct Heteromeric Fimbriae in Actinomyces naeslundii. J. Bacteriol.
189: 3156-3165
[Abstract]
[Full Text]
-
Bentley, M. L., Gaweska, H., Kielec, J. M., McCafferty, D. G.
(2007). Engineering the Substrate Specificity of Staphylococcus aureus Sortase A: THE beta6/beta7 LOOP FROM SrtB CONFERS NPQTN RECOGNITION TO SrtA. J. Biol. Chem.
282: 6571-6581
[Abstract]
[Full Text]
-
Severin, A., Nickbarg, E., Wooters, J., Quazi, S. A., Matsuka, Y. V., Murphy, E., Moutsatsos, I. K., Zagursky, R. J., Olmsted, S. B.
(2007). Proteomic Analysis and Identification of Streptococcus pyogenes Surface-Associated Proteins. J. Bacteriol.
189: 1514-1522
[Abstract]
[Full Text]
-
Lizano, S., Luo, F., Bessen, D. E.
(2007). Role of Streptococcal T Antigens in Superficial Skin Infection. J. Bacteriol.
189: 1426-1434
[Abstract]
[Full Text]
-
Torres, V. J., Pishchany, G., Humayun, M., Schneewind, O., Skaar, E. P.
(2006). Staphylococcus aureus IsdB Is a Hemoglobin Receptor Required for Heme Iron Utilization. J. Bacteriol.
188: 8421-8429
[Abstract]
[Full Text]
-
Maresso, A. W., Chapa, T. J., Schneewind, O.
(2006). Surface Protein IsdC and Sortase B Are Required for Heme-Iron Scavenging of Bacillus anthracis. J. Bacteriol.
188: 8145-8152
[Abstract]
[Full Text]
-
Swierczynski, A., Ton-That, H.
(2006). Type III Pilus of Corynebacteria: Pilus Length Is Determined by the Level of Its Major Pilin Subunit.. J. Bacteriol.
188: 6318-6325
[Abstract]
[Full Text]
-
Itoi, Y., Horinaka, M., Tsujimoto, Y., Matsui, H., Watanabe, K.
(2006). Characteristic Features in the Structure and Collagen-Binding Ability of a Thermophilic Collagenolytic Protease from the Thermophile Geobacillus collagenovorans MO-1.. J. Bacteriol.
188: 6572-6579
[Abstract]
[Full Text]