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Microbiology and Molecular Biology Reviews, December 2004, p. 771-795, Vol. 68, No. 4
1092-2172/04/$08.00+0 DOI: 10.1128/MMBR.68.4.771-795.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
Process of Protein Transport by the Type III Secretion System
Partho Ghosh*
Department of Chemistry & Biochemistry, University of CaliforniaSan Diego, La Jolla, California
The type III secretion system (TTSS) of gram-negative bacteria is responsible for delivering bacterial proteins, termed effectors, from the bacterial cytosol directly into the interior of host cells. The TTSS is expressed predominantly by pathogenic bacteria and is usually used to introduce deleterious effectors into host cells. While biochemical activities of effectors vary widely, the TTSS apparatus used to deliver these effectors is conserved and shows functional complementarity for secretion and translocation. This review focuses on proteins that constitute the TTSS apparatus and on mechanisms that guide effectors to the TTSS apparatus for transport. The TTSS apparatus includes predicted integral inner membrane proteins that are conserved widely across TTSSs and in the basal body of the bacterial flagellum. It also includes proteins that are specific to the TTSS and contribute to ring-like structures in the inner membrane and includes secretin family members that form ring-like structures in the outer membrane. Most prominently situated on these coaxial, membrane-embedded rings is a needle-like or pilus-like structure that is implicated as a conduit for effector translocation into host cells. A short region of mRNA sequence or protein sequence in effectors acts as a signal sequence, directing proteins for transport through the TTSS. Additionally, a number of effectors require the action of specific TTSS chaperones for efficient and physiologically meaningful translocation into host cells. Numerous models explaining how effectors are transported into host cells have been proposed, but understanding of this process is incomplete and this topic remains an active area of inquiry.
* Mailing address: Department of Chemistry & Biochemistry, 0375, 9500 Gilman Dr., University of CaliforniaSan Diego, La Jolla, CA 92093-0314. Phone: (858) 822-1139. Fax (858) 534-7042. E-mail:
pghosh{at}ucsd.edu.
Microbiology and Molecular Biology Reviews, December 2004, p. 771-795, Vol. 68, No. 4
1092-2172/04/$08.00+0 DOI: 10.1128/MMBR.68.4.771-795.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
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[Full Text]
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[Abstract]
[Full Text]
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[Full Text]
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[Abstract]
[Full Text]