The type III secretion injectisome (original) (raw)

• Cornelis, G. R. & Wolf-Watz, H. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23, 861–867 (1997).
  CAS PubMed Google Scholar
• Galan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).
  CAS PubMed Google Scholar
• Cornelis, G. R. & Van Gijsegem, F. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54, 735–774 (2000).
  CAS PubMed Google Scholar
• Mota, L. J. & Cornelis, G. R. The bacterial injection kit: type III secretion systems. Ann. Med. 37, 234–249 (2005).
  CAS PubMed Google Scholar
• Alfano, J. R. & Collmer, A. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42, 385–414 (2004).
  CAS PubMed Google Scholar
• Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M. & Dangl, J. L. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 5 June 2006 [epub ahead of print].
• Yip, C. K. & Strynadka, N. C. New structural insights into the bacterial type III secretion system. Trends Biochem. Sci. 31, 223–230 (2006).
  CAS PubMed Google Scholar
• Van Gijsegem, F. et al. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15, 1095–1114 (1995).
  CAS PubMed Google Scholar
• Fields, K. A., Plano, G. V. & Straley, S. C. A low-Ca2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J. Bacteriol. 176, 569–579 (1994).
  CAS PubMed PubMed Central Google Scholar
• Woestyn, S., Allaoui, A., Wattiau, P. & Cornelis, G. R. YscN, the putative energizer of the Yersinia Yop secretion machinery. J. Bacteriol. 176, 1561–1569 (1994).
  CAS PubMed PubMed Central Google Scholar
• Macnab, R. M. How bacteria assemble flagella. Annu. Rev. Microbiol. 57, 77–100 (2003).
  CAS PubMed Google Scholar
• Young, G. M., Schmiel, D. H. & Miller, V. L. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl Acad. Sci. USA 96, 6456–6461 (1999).
  CAS PubMed PubMed Central Google Scholar
• Kubori, T. et al. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602–605 (1998).
  CAS PubMed Google Scholar
• Gophna, U., Ron, E. Z. & Graur, D. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312, 151–163 (2003).
  CAS PubMed Google Scholar
• Pallen, M. J., Beatson, S. A. & Bailey, C. M. Bioinformatics, genomics and evolution of non-flagellar type III secretion systems: a Darwinian perspective. FEMS Microbiol. Rev. 29, 201–229 (2005).
  CAS PubMed Google Scholar
• Troisfontaines, P. & Cornelis, G. R. Type III secretion: more systems than you think. Physiology (Bethesda) 20, 326–339 (2005).
  CAS Google Scholar
• Roy-Burman, A. et al. Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J. Infect. Dis. 183, 1767–1774 (2001).
  CAS PubMed Google Scholar
• Burr, S. E., Wahli, T., Segner, H., Pugovkin, D. & Frey, J. Association of type III secretion genes with virulence of Aeromonas salmonicida subsp. salmonicida. Dis. Aquat. Organ. 57, 167–171 (2003).
  CAS PubMed Google Scholar
• Zhou, D. & Galan, J. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect. 3, 1293–1298 (2001).
  CAS PubMed Google Scholar
• Waterman, S. R. & Holden, D. W. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 5, 501–511 (2003).
  CAS PubMed Google Scholar
• Sekiya, K. et al. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc. Natl Acad. Sci. USA 98, 11638–11643 (2001).
  CAS PubMed PubMed Central Google Scholar
• Tamano, K. et al. Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J. 19, 3876–3887 (2000).
  CAS PubMed PubMed Central Google Scholar
• Blocker, A. et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147, 683–693. (1999).
  CAS PubMed PubMed Central Google Scholar
• Kimbrough, T. G. & Miller, S. I. Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc. Natl Acad. Sci. USA 97, 11008–11013 (2000).
  CAS PubMed PubMed Central Google Scholar
• Daniell, S. J. et al. The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell Microbiol. 3, 865–871 (2001).
  CAS PubMed Google Scholar
• Ogino, T. et al. Assembly of the type III secretion apparatus of enteropathogenic Escherichia coli. J. Bacteriol. 188, 2801–2811 (2006).
  CAS PubMed PubMed Central Google Scholar
• Morita-Ishihara, T. et al. Shigella Spa33 is an essential C-ring component of type III secretion machinery. J. Biol. Chem. 281, 599–607 (2006).
  CAS PubMed Google Scholar
• Blocker, A. et al. Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol. Microbiol. 39, 652–663 (2001).
  CAS PubMed Google Scholar
• Feldman, M. F., Muller, S., Wuest, E. & Cornelis, G. R. SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol. Microbiol. 46, 1183–1197 (2002).
  CAS PubMed Google Scholar
• Marlovits, T. C. et al. Structural insights into the assembly of the type III secretion needle complex. Science 306, 1040–1042 (2004).
  CAS PubMed PubMed Central Google Scholar
• Young, H. S., Dang, H., Lai, Y., DeRosier, D. J. & Khan, S. Variable symmetry in Salmonella typhimurium flagellar motors. Biophys. J. 84, 571–577 (2003).
  CAS PubMed PubMed Central Google Scholar
• Bogdanove, A. J. et al. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20, 681–683 (1996).
  CAS PubMed Google Scholar
• Kubori, T., Sukhan, A., Aizawa, S. I. & Galan, J. E. Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc. Natl Acad. Sci. USA 97, 10225–10230 (2000).
  CAS PubMed PubMed Central Google Scholar
• Koster, M. et al. The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol. Microbiol. 26, 789–797 (1997).
  CAS PubMed Google Scholar
• Burghout, P. et al. Structure and electrophysiological properties of the YscC secretin from the type III secretion system of Yersinia enterocolitica J. Bacteriol. 186, 4645–4654 (2004).
  CAS PubMed PubMed Central Google Scholar
• Chami, M. et al. Structural insights into the secretin PulD and its trypsin-resistant core. J. Biol. Chem. 280, 37732–37741 (2005).
  CAS PubMed Google Scholar
• Collins, R. F. et al. Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 A resolution. J. Biol. Chem. 279, 39750–39756 (2004).
  CAS PubMed Google Scholar
• Russel, M. Phage assembly: a paradigm for bacterial virulence factor export? Science 265, 612–614 (1994).
  CAS PubMed Google Scholar
• Burghout, P. et al. Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. J. Bacteriol. 186, 5366–5375 (2004).
  CAS PubMed PubMed Central Google Scholar
• Daefler, S. & Russel, M. The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG. Mol. Microbiol. 28, 1367–1380 (1998).
  CAS PubMed Google Scholar
• Crago, A. M. & Koronakis, V. Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol. Microbiol. 30, 47–56 (1998).
  CAS PubMed Google Scholar
• Crepin, V. F. et al. Structural and functional studies of the enteropathogenic Escherichia coli type III needle complex protein EscJ. Mol. Microbiol. 55, 1658–1670 (2005).
  CAS PubMed Google Scholar
• Yip, C. K. et al. Structural characterization of the molecular platform for type III secretion system assembly. Nature 435, 702–707 (2005).
  CAS PubMed Google Scholar
• Sukhan, A., Kubori, T. & Galan, J. E. Synthesis and localization of the Salmonella SPI-1 type III secretion needle complex proteins PrgI and PrgJ. J. Bacteriol. 185, 3480–3483 (2003).
  CAS PubMed PubMed Central Google Scholar
• Fadouloglou, V. E. et al. Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems. Proc. Natl Acad. Sci. USA 101, 70–75 (2004).
  CAS PubMed Google Scholar
• Gonzalez-Pedrajo, B., Fraser, G. M., Minamino, T. & Macnab, R. M. Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Mol. Microbiol. 45, 967–982 (2002).
  CAS PubMed Google Scholar
• Jackson, M. W. & Plano, G. V. Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol. Lett. 186, 85–90 (2000).
  CAS PubMed Google Scholar
• Blaylock, B., Riordan, K. E., Missiakas, D. M. & Schneewind, O. Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL. J. Bacteriol. 188, 3525–3534 (2006).
  CAS PubMed PubMed Central Google Scholar
• Jouihri, N. et al. MxiK and MxiN interact with the Spa47 ATPase and are required for transit of the needle components MxiH and MxiI, but not of Ipa proteins, through the type III secretion apparatus of Shigella flexneri. Mol. Microbiol. 49, 755–767 (2003).
  CAS PubMed Google Scholar
• Minamino, T. & MacNab, R. M. Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol. Microbiol. 35, 1052–1064 (2000).
  CAS PubMed Google Scholar
• Pozidis, C. et al. Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. J. Biol. Chem. 278, 25816–25824 (2003).
  CAS PubMed Google Scholar
• Muller, S. A. et al. Double hexameric ring assembly of the type III protein translocase ATPase HrcN. Mol. Microbiol. 61, 119–125 (2006).
  CAS PubMed Google Scholar
• Claret, L., Calder, S. R., Higgins, M. & Hughes, C. Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol. Microbiol. 48, 1349–1355 (2003).
  CAS PubMed PubMed Central Google Scholar
• Akeda, Y. & Galan, J. E. Chaperone release and unfolding of substrates in type III secretion. Nature 437, 911–915 (2005).
  CAS PubMed Google Scholar
• Hoiczyk, E. & Blobel, G. Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc. Natl Acad. Sci. USA 98, 4669–4674 (2001).
  CAS PubMed PubMed Central Google Scholar
• Cordes, F. S. et al. Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem 278, 17103–7 (2003).
  CAS PubMed Google Scholar
• Deane, J. E. et al. Molecular model of a type III secretion system needle: implications for host-cell sensing. Proc. Natl Acad. Sci. USA (2006).
• Yonekura, K., Maki-Yonekura, S. & Namba, K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424, 643–650 (2003).
  CAS PubMed Google Scholar
• Mueller, C. A. et al. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310, 674–676 (2005).
  CAS PubMed Google Scholar
• Derewenda, U. et al. The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure (Camb) 12, 301–306 (2004).
  CAS Google Scholar
• Jin, Q. & He, S. Y. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294, 2556–2558 (2001).
  CAS PubMed Google Scholar
• Hakansson, S., Galyov, E. E., Rosqvist, R. & Wolf-Watz, H. The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane. Mol. Microbiol. 20, 593–603. (1996).
  CAS PubMed Google Scholar
• Neyt, C. & Cornelis, G. R. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol. Microbiol. 33, 971–981 (1999).
  CAS PubMed Google Scholar
• Rosqvist, R., Magnusson, K. E. & Wolf-Watz, H. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13, 964–972 (1994).
  CAS PubMed PubMed Central Google Scholar
• Sory, M. P. & Cornelis, G. R. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14, 583–594 (1994).
  CAS PubMed Google Scholar
• Pettersson, J. et al. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32, 961–976 (1999).
  CAS PubMed Google Scholar
• Boland, A. et al. Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5–1. 8 macrophages by the YopB, D, N delivery apparatus. EMBO J. 15, 5191–5201 (1996).
  CAS PubMed PubMed Central Google Scholar
• Sarker, M. R., Neyt, C., Stainier, I. & Cornelis, G. R. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J. Bacteriol. 180, 1207–1214 (1998).
  CAS PubMed PubMed Central Google Scholar
• Menard, R., Sansonetti, P., Parsot, C. & Vasselon, T. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79, 515–525 (1994).
  CAS PubMed Google Scholar
• Harrington, A. et al. Characterization of the interaction of single tryptophan containing mutants of IpaC from Shigella flexneri with phospholipid membranes. Biochemistry 45, 626–636 (2006).
  CAS PubMed Google Scholar
• Hume, P. J., McGhie, E. J., Hayward, R. D. & Koronakis, V. The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol. Microbiol. 49, 425–439 (2003).
  CAS PubMed Google Scholar
• Schoehn, G. et al. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J. 22, 4957–4967 (2003).
  CAS PubMed PubMed Central Google Scholar
• Faudry, E., Vernier, G., Neumann, E., Forge, V. & Attree, I. Synergistic pore formation by type III toxin translocators of Pseudomonas aeruginosa. Biochemistry 45, 8117–8123 (2006).
  CAS PubMed Google Scholar
• Fields, K. A., Nilles, M. L., Cowan, C. & Straley, S. C. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67, 5395–5408 (1999).
  CAS PubMed PubMed Central Google Scholar
• Marenne, M. N., Journet, L., Mota, L. J. & Cornelis, G. R. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, yscF and YopN. Microb. Pathogen. 35, 243–258 (2003).
  CAS Google Scholar
• Hakansson, S. et al. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15, 5812–5823. (1996).
  CAS PubMed PubMed Central Google Scholar
• Goure, J. et al. The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect. Immun. 72, 4741–4750 (2004).
  CAS PubMed PubMed Central Google Scholar
• Goure, J., Broz, P., Attree, O., Cornelis, G. R. & Attree, I. Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J. Infect. Dis. 192, 218–225 (2005).
  CAS PubMed Google Scholar
• Picking, W. L. et al. IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes. Infect. Immun. 73, 1432–1440 (2005).
  CAS PubMed PubMed Central Google Scholar
• Espina, M. et al. IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect. Immun. 74, 4391–4400 (2006).
  CAS PubMed PubMed Central Google Scholar
• Warawa, J., Finlay, B. B. & Kenny, B. Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli. Infect. Immun. 67, 5538–5540 (1999).
  CAS PubMed PubMed Central Google Scholar
• Yonekura, K. et al. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290, 2148–2152 (2000).
  CAS PubMed Google Scholar
• Li, C. M. et al. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J. 21, 1909–1915 (2002).
  CAS PubMed PubMed Central Google Scholar
• Crepin, V. F., Shaw, R., Abe, C. M., Knutton, S. & Frankel, G. Polarity of enteropathogenic Escherichia coli EspA filament assembly and protein secretion. J. Bacteriol. 187, 2881–2889 (2005).
  CAS PubMed PubMed Central Google Scholar
• Marlovits, T. C. et al. Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441, 637–640 (2006).
  CAS PubMed Google Scholar
• Ikeda, T., Asakura, S. & Kamiya, R. 'Cap' on the tip of Salmonella flagella. J. Mol. Biol. 184, 735–737 (1985).
  CAS PubMed Google Scholar
• Quinaud, M. et al. The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa. J. Biol. Chem. 280, 36293–36300 (2005).
  CAS PubMed Google Scholar
• Journet, L., Agrain, C., Broz, P. & Cornelis, G. R. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302, 1757–1760 (2003).
  CAS PubMed Google Scholar
• Williams, A. W. et al. Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J. Bacteriol. 178, 2960–2970 (1996).
  CAS PubMed PubMed Central Google Scholar
• Magdalena, J. et al. Spa32 regulates a switch in substrate specificity of the type III secreton of Shigella flexneri from needle components to Ipa proteins. J. Bacteriol. 184, 3433–3441 (2002).
  CAS PubMed PubMed Central Google Scholar
• Makishima, S., Komoriya, K., Yamaguchi, S. & Aizawa, S. I. Length of the flagellar hook and the capacity of the type III export apparatus. Science 291, 2411–2413 (2001).
  CAS PubMed Google Scholar
• Agrain, C. et al. Characterization of a type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol. Microbiol. 56, 54–67 (2005).
  CAS PubMed Google Scholar
• Agrain, C., Sorg, I., Paroz, C. & Cornelis, G. R. Secretion of YscP from Yersinia enterocolitica is essential to control the length of the injectisome needle but not to change the type III secretion substrate specificity. Mol. Microbiol. 57, 1415–1427 (2005).
  CAS PubMed Google Scholar
• Creighton, T. E. Proteins: structures and molecular properties 2nd edn (W. H. Freeman, New York, 1992).
  Google Scholar
• Kutsukake, K., Minamino, T. & Yokoseki, T. Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J. Bacteriol. 176, 7625–7629 (1994).
  CAS PubMed PubMed Central Google Scholar
• Hirano, T., Yamaguchi, S., Oosawa, K. & Aizawa, S. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176, 5439–5449 (1994).
  CAS PubMed PubMed Central Google Scholar
• Edqvist, P. J. et al. YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J. Bacteriol. 185, 2259–2266 (2003).
  CAS PubMed PubMed Central Google Scholar
• Minamino, T. et al. Domain organization and function of Salmonella FliK, a flagellar hook-length control protein. J. Mol. Biol. 341, 491–502 (2004).
  CAS PubMed Google Scholar
• Minamino, T. & Macnab, R. M. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 182, 4906–4914 (2000).
  CAS PubMed PubMed Central Google Scholar
• Moriya, N., Minamino, T., Hughes, K. T., Macnab, R. M. & Namba, K. The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J. Mol. Biol. 359, 466–477 (2006).
  CAS PubMed Google Scholar
• Tamano, K., Katayama, E., Toyotome, T. & Sasakawa, C. Shigella Spa32 is an essential secretory protein for functional type III secretion machinery and uniformity of its needle length. J. Bacteriol. 184, 1244–1252 (2002).
  CAS PubMed PubMed Central Google Scholar
• Chakravortty, D., Rohde, M., Jager, L., Deiwick, J. & Hensel, M. Formation of a novel surface structure encoded by Salmonella pathogenicity island 2. EMBO J. 24, 2043–2052 (2005).
  CAS PubMed PubMed Central Google Scholar
• Mota, L. J., Journet, L., Sorg, I., Agrain, C. & Cornelis, G. R. Bacterial injectisomes: needle length does matter. Science 307, 1278 (2005).
  PubMed Google Scholar
• West, N. P. et al. Optimization of virulence functions through glucosylation of Shigella LPS. Science 307, 1313–1317 (2005).
  CAS PubMed Google Scholar
• Pettersson, J. et al. Modulation of virulence factor expression by pathogen target cell contact. Science 273, 1231–1233 (1996).
  CAS PubMed Google Scholar
• Forsberg, A., Viitanen, A. M., Skurnik, M. & Wolf-Watz, H. The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol. Microbiol. 5, 977–986 (1991).
  CAS PubMed Google Scholar
• Day, J. B. & Plano, G. V. A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol. Microbiol. 30, 777–788 (1998).
  CAS PubMed Google Scholar
• Iriarte, M. & Cornelis, G. R. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29, 915–929 (1998).
  CAS PubMed Google Scholar
• Skryzpek, E. & Straley, S. C. LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis. J. Bacteriol. 175, 3520–3528 (1993).
  CAS PubMed PubMed Central Google Scholar
• Schubot, F. D. et al. Three-dimensional structure of a macromolecular assembly that regulates type III secretion in Yersinia pestis. J. Mol. Biol. 346, 1147–1161 (2005).
  CAS PubMed Google Scholar
• Nilles, M. L., Williams, A. W., Skrzypek, E. & Straley, S. C. Yersinia pestis LcrV forms a stable complex with LcrG and may have a secretion-related regulatory role in the low-Ca2+ response. J. Bacteriol. 179, 1307–1316 (1997).
  CAS PubMed PubMed Central Google Scholar
• van der Goot, F. G., Tran van Nhieu, G., Allaoui, A., Sansonetti, P. & Lafont, F. Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism. J. Biol. Chem. 279, 47792–47798 (2004).
  CAS PubMed Google Scholar
• Hayward, R. D. et al. Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol. Microbiol. 56, 590–603 (2005).
  CAS PubMed Google Scholar
• Kenjale, R. et al. The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J. Biol. Chem. 280, 42929–42937 (2005).
  CAS PubMed Google Scholar
• Andersson, K. et al. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol. Microbiol. 20, 1057–10569 (1996).
  CAS PubMed Google Scholar
• Schlumberger, M. C. et al. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc. Natl Acad. Sci. USA 102, 12548–12553 (2005).
  CAS PubMed PubMed Central Google Scholar
• Enninga, J., Mounier, J., Sansonetti, P. & Tran Van Nhieu, G. Secretion of type III effectors into host cells in real time. Nature Methods 2, 959–965 (2005).
  CAS PubMed Google Scholar
• Cornelis, G. R., Agrain, C. & Sorg, I. Length control of extended protein structures in bacteria and bacteriophages. Curr. Opin. Microbiol. 9, 201–206 (2006).
  CAS PubMed Google Scholar
• Evdokimov, A. G. et al. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nature Struct. Biol. 10, 789–793 (2003).
  CAS PubMed Google Scholar
• Birtalan, S. & Ghosh, P. Structure of the Yersinia type III secretory system chaperone SycE. Nature Struct. Biol. 8, 974–978 (2001).
  CAS PubMed Google Scholar
• Birtalan, S. C., Phillips, R. M. & Ghosh, P. Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol. Cell. 9, 971–980 (2002).
  CAS PubMed Google Scholar
• Stebbins, C. E. & Galan, J. E. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414, 77–81 (2001).
  CAS PubMed Google Scholar
• Fraser, G. M., Bennett, J. C. & Hughes, C. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol. Microbiol. 32, 569–580 (1999).
  CAS PubMed Google Scholar
• Auvray, F., Thomas, J., Fraser, G. M. & Hughes, C. Flagellin polymerisation control by a cytosolic export chaperone. J. Mol. Biol. 308, 221–229 (2001).
  CAS PubMed PubMed Central Google Scholar
• Bennett, J. C. & Hughes, C. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8, 202–204 (2000).
  CAS PubMed Google Scholar
• Neyt, C. & Cornelis, G. R. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol. Microbiol. 31, 143–156 (1999).
  CAS PubMed Google Scholar
• Wattiau, P., Bernier, B., Deslee, P., Michiels, T. & Cornelis, G. R. Individual chaperones required for Yop secretion by Yersinia. Proc. Natl Acad. Sci. USA 91, 10493–10497 (1994).
  CAS PubMed PubMed Central Google Scholar
• Darwin, K. H. & Miller, V. L. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J. 20, 1850–1862 (2001).
  CAS PubMed PubMed Central Google Scholar
• Page, A. L. & Parsot, C. Chaperones of the type III secretion pathway: jacks of all trades. Mol. Microbiol. 46, 1–11 (2002).
  CAS PubMed Google Scholar
• Feldman, M. F. & Cornelis, G. R. The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol. Lett. 219, 151–158 (2003).
  CAS PubMed Google Scholar
• Ghosh, P. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68, 771–795 (2004).
  CAS PubMed PubMed Central Google Scholar
• Parsot, C., Hamiaux, C. & Page, A. L. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6, 7–14 (2003).
  CAS PubMed Google Scholar
• Wattiau, P. & Cornelis, G. R. SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol. Microbiol. 8, 123–131 (1993).
  CAS PubMed Google Scholar
• Luo, Y. et al. Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nature Struct. Biol. 8, 1031–1036 (2001).
  CAS PubMed Google Scholar
• Evdokimov, A. G., Tropea, J. E., Routzahn, K. M. & Waugh, D. S. Three-dimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr. D Biol. Crystallogr. 58, 398–406 (2002).
  PubMed Google Scholar
• Locher, M. et al. Crystal Structure of the Yersinia enterocolitica type III secretion chaperone SycT. J. Biol. Chem. 280, 31149–31155 (2005).
  CAS PubMed Google Scholar
• Trame, C. B. & McKay, D. B. Structure of the Yersinia enterocolitica molecular-chaperone protein SycE. Acta Crystallogr. D Biol. Crystallogr. 59, 389–392 (2003).
  PubMed Google Scholar
• Phan, J., Tropea, J. E. & Waugh, D. S. Structure of the Yersinia pestis type III secretion chaperone SycH in complex with a stable fragment of YscM2. Acta Crystallogr. D Biol. Crystallogr. 60, 1591–1599 (2004).
  PubMed Google Scholar
• van Eerde, A., Hamiaux, C., Perez, J., Parsot, C. & Dijkstra, B. W. Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep. 5, 477–483 (2004).
  CAS PubMed PubMed Central Google Scholar
• Buttner, C. R., Cornelis, G. R., Heinz, D. W. & Niemann, H. H. Crystal structure of Yersinia enterocolitica type III secretion chaperone SycT. Protein Sci. 14, 1993–2002 (2005).
  PubMed PubMed Central Google Scholar
• Boyd, A. P., Lambermont, I. & Cornelis, G. R. Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J. Bacteriol. 182, 4811–4821 (2000).
  CAS PubMed PubMed Central Google Scholar
• Page, A. L., Sansonetti, P. & Parsot, C. Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol. Microbiol. 43, 1533–1542 (2002).
  CAS PubMed Google Scholar
• Letzelter, M. et al. The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J. 25, 3223–3233 (2006).
  CAS PubMed PubMed Central Google Scholar
• Swietnicki, W. et al. Novel protein-protein interactions of the Yersinia pestis type III secretion system elucidated with a matrix analysis by surface plasmon resonance and mass spectrometry. J. Biol. Chem. 279, 38693–38700 (2004).
  CAS PubMed Google Scholar
• Krall, R., Zhang, Y. & Barbieri, J. T. Intracellular membrane localization of pseudomonas ExoS and Yersinia YopE in mammalian cells. J. Biol. Chem. 279, 2747–2753 (2004).
  CAS PubMed Google Scholar
• Ehrbar, K., Hapfelmeier, S., Stecher, B. & Hardt, W. D. InvB is required for type III-dependent secretion of SopA in Salmonella enterica serovar Typhimurium. J. Bacteriol. 186, 1215–1219 (2004).
  CAS PubMed PubMed Central Google Scholar
• Creasey, E. A. et al. CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol. Microbiol. 47, 209–221 (2003).
  CAS PubMed Google Scholar
• Lee, S. H. & Galan, J. E. Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51, 483–495 (2004).
  CAS PubMed Google Scholar
• Wulff-Strobel, C. R., Williams, A. W. & Straley, S. C. LcrQ and SycH function together at the Ysc type III secretion system in Yersinia pestis to impose a hierarchy of secretion. Mol. Microbiol. 43, 411–423 (2002).
  CAS PubMed Google Scholar
• Parsot, C. et al. A secreted anti-activator, OspD1, and its chaperone, Spa15, are involved in the control of transcription by the type III secretion apparatus activity in Shigella flexneri. Mol. Microbiol. 56, 1627–1635 (2005).
  CAS PubMed Google Scholar
• Hanson, P. I. & Whiteheart, S. W. AAA+ proteins: have engine, will work. Nature Rev. Mol. Cell Biol. 6, 519–529 (2005).
  CAS Google Scholar
• Yip, C.K., Finlay, B.B. & Strynadka, N.C. Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nature Struct. Mol. Biol. 12, 75–81 (2005).
  CAS Google Scholar
• Kauppi, A. M., Nordfelth, R., Uvell, H., Wolf-Watz, H. & Elofsson, M. Targeting bacterial virulence: inhibitors of type III secretion in Yersinia. Chem. Biol. 10, 241–249 (2003).
  CAS PubMed Google Scholar
• Wolf, K. et al. Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol. Microbiol. 61, 1543–1555 (2006).
  CAS PubMed PubMed Central Google Scholar
• Muschiol, S. et al. A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. Proc. Natl Acad. Sci. USA 103, 14566–14571 (2006).
  CAS PubMed PubMed Central Google Scholar