Type III secretion: A bacterial device for close combat with cells of their eukaryotic host

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 355, Issue 1397, 2000, Pages 681-693

  Cornelis, Guy R ^a,b  

^a DE DUVE INSTITUTE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Bacterial pathogenesis; Enteropathogenic E. coli; Salmonella; Shigella; Translocation; Yersinia

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SALMONELLA; SHIGELLA; YERSINIA;

EID: 0034729212     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2000.0608     Document Type: Article

References (113)

1. Abe, A., de Grado, M., Pfuetzner, R. A., Sanchez-SanMartin, C., DeVinney, R., Puente, J. L., Strynadka, N. C. J. & Finlay, B. B. 1999 Enteropathogenic Escherichia coli translocated intimin receptor, Tir, requires a specific chaperone for stable secretion. Mol. Microbiol. 33, 1162-1175.
2. Anderson, D. M. & Schneewind, O. 1997 A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278, 1140-1143.
3. Anderson, D. M. & Schneewind, O. 1999a Type III machines of gram-negative pathogens: injecting virulence factors into host cells and more. Curr. Opin. Microbiol. 2, 18-24.
4. Anderson, D. M. & Schneewind, O. 1999b Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol. Microbiol. 31, 1139-1148.
5. Blocker, A., Gounon, P., Larquet, E., Allaoui, A., Niebuhr, K., Cabiaux, V., Parsot, C. & Sansonetti, P. 1999 Role of Shigella's type III secretion system in insertion of IpaB and IpaC into the host membrane. J. Cell Biol. 147, 683-693.
6. Boland, A. & Cornelis, G. R. 1998 Role of YopP in suppression of tumour necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66, 1878-1884.
7. Boland, A., Sory, M. P., Iriarte, M., Kerbourch, C., Wattiau, P. & Cornelis, G. R. 1996 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.
8. Boyd, A. P., Sory, M. P., Iriarte, M. & Cornelis, G. R. 1998 Heparin interferes with translocation of Yop proteins into HeLa cells and binds to LcrG, a regulatory component of the Yersinia Yop apparatus. Mol. Microbiol. 27, 425-436.
9. Boyd, A. P. et al. 2000 Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain. (In preparation.)
10. Burrows, T. W. & Bacon, G. A. 1958 The effects of loss of different virulence determinants on the virulence and immunogenicity of strains of Pasteurella pestis. Br. J. Exp. Pathol. 39, 278-291.
11. Chaux, P. (and 10 others) 1999 Identification of five Mage-AI epitopes recognized by cytolytic T lymphocytes obtained by in vitro stimulation with dendritic cells transduced with Mage-AI. J. Immunol. 163, 2928-2936.
12. Chen, Y., Smith, M. R., Thirumalai, K. & Zychlinsky, A. 1996 A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 15, 3853-3860.
13. Cheng, L. W., Anderson, D. M. & Schneewind, O. 1997 Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol. Microbiol. 24, 757-765.
14. Cornelis, G. R. 1998 The Yersinia deadly kiss. J. Bacteriol. 180, 5495-5504.
15. Cornelis, G. R. & Wolf-Watz, H. 1997 The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23, 861-867.
16. Cornelis, G. R., Boland, A., Boyd, A. P., Geuijen, C., Iriarte, M., Neyt, C., Sory, M.-P. & Stainier, I. 1998 The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62, 1315-1352.
17. Covacci, A., Telford, J. L., Del Giudice, G., Parsonnet, J. & Rappuoli, R. 1999 Helicobacter pylori virulence and genetic geography. Science 284, 1328-1333.
18. Day, J. B. & Plano, G. V. 1998 A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol. Microbiol. 30, 777-788.
19. Deibel, C., Krämer, S., Chakraborty, T. & Ebel, F. 1998 EspE, a novel secreted protein of attaching and effacing bacteria, is directly translocated into infected host cells, where it appears as a tyrosine-phosphorylated 90 kDa protein. Mol. Microbiol. 28, 463-474.
20. Elliott, S. J., Wainwright, L. A., McDaniel, T. K., Jarvis, K. G., Deng, Y., Lai, L., McNamara, B. P., Donnenberg, M. S. & Kaper, J. B. 1998 The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28, 1-4.
21. Elliott, S. J., Hutcheson, S. W., Dubois, M. S., Mellies, J. L., Wainwright, L. A., Batchelor, M., Frankel, G., Knutton, S. & Kaper, J. B. 1999 Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol. Microbiol. 33, 1176-1189.
22. Fekkes, P. & Driessen, A. J. M. 1999 Protein targeting to the bacterial cytoplasmic membrane. Microbiol. Mol. Biol. Rev. 63, 161-173.
23. Finck-Barbançon, V., Goranson, J., Zhu, L., Sawa, T., Wiener Kronish, J. P., Fleiszig, S. M. J., Wu, C., Mend Mueller, L. & Frank, D. W. 1997 ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol. 25, 547-557.
24. Finck-Barbançon, V., Yahr, T. L. & Frank, D. W. 1998 Identification and characterization of SpcU, a chaperone required for efficient secretion of the ExoU cytotoxin. J. Bacteriol. 180, 6224-6231.
25. Francis, M. S. & Wolf-Watz, H. 1998 YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 29, 799-813.
26. Frankel, G., Phillips, A. D., Rosenshine, I., Dougan, G., Kaper, J. B. & Knutton, S. 1998 Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30, 911-921.
27. Fraser, G. M., Bennett, J. C. Q. & Hughes, C. 1999 Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol. Microbiol. 32, 569-580.
28. Frithz-Lindsten, E., Rosqvist, R., Johansson, L. & Forsberg, A. 1995 The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensible for targeting to the secretion loci. Mol. Microbiol. 16, 635-647.
29. Frithz-Lindsten, E., Du, Y., Rosqvist, R. & Forsberg, A. 1997 Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol. Microbiol. 25, 1125-1139.
30. Fu, Y. X. & Galan, J. E. 1998 Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J. Bacteriol. 180, 3393-3399.
31. Galan, J. E. 1998 Interactions of Salmonella with host cells: encounters of the closest kind. Proc. Natl Acad. Sci. USA 95, 14006-14008.
32. Galan, J. E. & Collmer, A. 1999 Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322-1328.
33. Genin, S. & Boucher, C. A. 1994 A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet. 243, 112-118.
34. Ginocchio, C. C., Olmsted, S. B., Wells, C. L. & Galan, J. E. 1994 Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76, 717-724.
35. Goosney, D. L., de Grado, M. & Finlay, B. B. 1999 Putting E-coli on a pedestal: a unique system to study signal transduction and the actin cytoskeleton. Trends Cell Biol. 9, 11-14.
36. Håkansson, S., Galyov, E. E., Rosqvist, R. & Wolf-Watz, H. 1996a 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.
37. Håkansson, S., Schesser, K., Persson, C., Galyov, E. E., Rosqvist, R., Homble, F. & Wolf-Watz, H. 1996b 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.
38. Hardt, W. D. & Galan, J. E. 1997 A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc. Natl Acad. Sci. USA 94, 9887-9892.
39. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galan, J. E. 1998a S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826.
40. Hardt, W. D., Urlaub, H. & Galan, J. E. 1998b A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc. Natl Acad. Sci. USA 95, 2574-2579.
41. Hauser, A. R., Kang, P. J. & Engel, J. N. 1998 PepA, a secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol. Microbiol. 27, 807-818.
42. Hayward, R. D. & Koronakis, V. 1999 Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18, 4926-4934.
43. Hensel, M., Shea, J. E., Raupach, B., Monack, D. M., Falkow, S., Gleeson, C., Kubo, T. & Holden, D. W. 1997 Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2. Mol. Microbiol. 24, 155-167.
44. Hensel, M., Shea, J. E., Waterman, S. R., Mundy, R., Nikolaus, T., Banks, G., Vazquez-Torres, A., Gleeson, C., Fang, F. C. & Holden, D. W. 1998 Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30, 163-174.
45. Hersh, D., Monack, D. M., Smith, M. R., Ghori, N., Falkow, S. & Zychlinsky, A. 1999 The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl Acad. Sci. USA 96, 2396-2401.
46. Higushi, K. & Smith, J. L. 1961 Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J. Bacteriol. 81, 605-608.
47. Hilbi, H., Moss, J. E., Hersh, D., Chen, Y. J., Arondel, J., Banerjee, S., Flavell, R. A., Yuan, J. Y., Sansonetti, P. J. & Zychlinsky, A. 1998 Shigella-induced apoptosis is dependent on caspase-I which binds to IpaB. J. Biol. Chem. 273, 32895-32900.
48. Hobbie, S., Chen, L. M., Davis, R. J. & Galan, J. E. 1997 Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 159, 5550-5559.
49. Iriarte, M. & Cornelis, G. R. 1998 YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29, 915-929.
50. Iriarte, M. & Corneles, G. R. 1999 Identification of SycN, YscX, and YscY, three new elements of the Yersinia Yop virulon. J. Bacteriol. 181, 675-680.
51. Jackson, M. W., Day, J. B. & Plano, G. V. 1998 YscB of Yersinia pestis functions as a specific chaperone for YopN. J. Bacteriol. 180, 4912-4921.
52. Jarvis, K. G., Giron, J. A., Jerse, A. E., McDaniel, T. K., Donnenberg, M. S. & Kaper, J. B. 1995 Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl Acad. Sci. USA 92, 7996-8000.
53. Jones, M. A., Wood, M. W., Mullan, P. B., Watson, P. R., Wallis, T. S. & Galyov, E. E. 1998 Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect. Immun. 66, 5799-5804.
54. Kaniga, K., Tucker, S., Trollinger, D. & Galan, J. E. 1995 Homologs of the shigella IpaB and IpaC invasins are required for Salmonella entry into host cells. J. Bacteriol. 177, 3965-3971.
55. Kaniga, K., Uralil, J., Bliska, J. B. & Galan, J. E. 1996 A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol. Microbiol. 21, 633-641.
56. Kaper, J. B. 1998 EPEC delivers the goods. Trends Microbiol. 6, 169-172.
57. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D. J., Frey, E. A. & Finlay, B. B. 1997 Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91, 511-520.
58. Kerr, J. R., Rigg, G. P., Matthews, R. C. & Burnie, J. P. 1999 The Bpel locus encodes type III secretion machinery in Bordetella pertussis. Microb. Pathogen. 27, 349-367.
59. Knutton, S., Rosenshine, I., Pallen, M. J., Nisan, I., Neves, B. C., Bain, C., Wolf, C., Dougan, G. & Frankel, G. 1998 A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17, 2166-2176.
60. Koster, M., Bitter, W., de Cock, H., Allaoui, A., Cornelis, G. R. & Tommassen, J. 1997 The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol. Microbiol. 26, 789-798.
61. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J. E. & Aizawa, S.-I. 1998 Supramolecular structure of the Salmonella typhimurium type III protein secrection system. Science 280, 602-605.
62. McGuffie, E. M., Frank, D. W., Vincent, T. S. & Olson, J. C. 1998 Modificiation of Ras in eukaryotic cells by Pseudomonas aeruginosa exoenzyme S. Infect. Immun. 66, 2607-2613.
63. Ménard, R., Sansonetti, P. J., Parsot, C. & Vasselon, T. 1994 Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79, 515-525.
64. Michiels, T., Wattiau, P., Brasseur, R., Ruysschaert, J. M. & Cornelis, G. R. 1990 Secretion of Yop proteins by Yersiniae. Infect. Immun. 58, 2840-2849.
65. Mills, S. D., Boland, A., Sory, M. P., Van der Smissen, P., Kerbourch, G., Finlay, B. B. & Cornelis, G. R. 1997 Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl Acad. Sci. USA 94, 12638-12643.
66. Monack, D. M., Mecsas, J., Ghori, N. & Falkow, S. 1997 Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl Acad. Sci. USA 94, 10385-10390.
67. Neyt, C. & Cornelis, G. R. 1999 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.
68. Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E. & Majerus, P. W. 1998 SopB, a protein required for virulence of Salmonella dublin, is an inositol phophate phosphatase. Proc. Natl Acad. Sci. USA 95, 14057-14059.
69. Ochman, H., Soncini, F. C., Solomon, F. & Groisman, E. A. 1996 Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl Acad. Sci. USA 93, 7800-7804.
70. Payne, P. L. & Straley, S. C. 1998 YscO of Yersinia pestis is a mobile core component of the Yop secretion system. J. Bacteriol. 180, 3882-3890.
71. Pederson, K. J., Vallis, A. J., Aktories, K., Frank, D. W. & Barbieri, J. T. 1999 The amino-terminal domain of Pseudomonas aeruginosa ExoS disrupts actin filaments via small-molecular-weight GTP-binding proteins. Mol. Microbiol. 32, 393-401.
72. Persson, C., Nordfelth, R., Holmström, A., Hakansson, S., Rosqvist, R. & Wolf-Watz, H. 1995 Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol. Microbiol. 18, 135-150.
73. Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16, 2307-2318.
74. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K. E. & Wolf-Watz, H. 1996 Modulation of virulence factor expression by pathogen target cell contact. Science 273, 1231-1233.
75. Pettersson, J., Holmström, A., Hill, J., Leary, S., Frithz-Lindsten, E., von Euler-Matell, A., Carlsson, E., Titball, R., Forsberg, A. & Wolf-Watz, H. 1999 The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32, 961-976.
76. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E. L., Kalkkinen, N., Romantschuk, M. & He, S. Y. 1997 Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl Acad. Sci. USA 94, 3459-3464.
77. Rosqvist, R., Forsberg, A. & Wolf-Watz, H. 1991 Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect. Immun. 59, 4562-4569.
78. Rosqvist, R., Magnusson, K. E. & Wolf-Watz, H. 1994 Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13, 964-972.
79. Rosqvist, R., Håkansson, S., Forsberg, A. & Wolf-Watz, H. 1995 Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J. 14, 4187-4195.
80. Ruckdeschel, K., Harb, S., Roggenkamp, A., Hornef, M., Zumbihl, R., Kohler, S., Heesemann, J. & Rouot, B. 1998 Yersinia enterocolitica impairs activation of transcription factor NF-κB: involvement in the induction of programmed cell death and in the suppression of the macrophage TNF-α production. J. Exp. Med. 187, 1069-1079.
81. Russel, M. 1994 Phage assembly: a paradigm for bacterial virulence factor export? Science 265, 612-614.
82. Russmann, H., Shams, H., Poblete, F., Fu, Y. X., Galan, J. E. & Donis, R. O. 1998 Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science 281, 565-568.
83. Salmond, G. P. & Reeves, P. J. 1993 Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18, 7-12.
84. Sarker, M. R., Neyt, C., Stainier, I. & Cornelis, G. R. 1998 The Yersinia Yop virulon: LerV is required for extrusion of the translocators YopB and YopD. J. Bacteriol. 180, 1207-1214.
85. Sawa, T., Yahr, T. L., Ohara, M., Kurahashi, K., Gropper, M. A., Wiener-Kronish, J. P. & Frank, D. W. 1999 Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat. Med. 5, 392-398.
86. Schesser, K., Spiik, A.-K., Dukuzumuremyi, J.-M., Neurath, M. F., Pettersson, S. & Wolf-Watz, H. 1998 The yopJ locus is required for Yersinia-mediated inhibition of NF-κB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 28, 1067-1079.
87. Schesser, K., Dukuzumuremyi, J. M., Cilio, C., Borg, S.,Wallis, T. S., Pettersson, S. & Galyov, E. E. 2000 The Salmonella YopJ-homologue AvrA does not possess YopJ-like activity. Microb. Pathogen. 28, 59-70.
88. Shea, J. E., Hensel, M., Gleeson, C. & Holden, D. W. 1996 Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl Acad. Sci. USA 93, 2593-2597.
89. Skrzypek, E., Cowan, C. & Straley, S. C. 1998 Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus. Mol. Microbiol. 30, 1051-1065.
90. Sory, M. P. & Cornelis, G. R. 1994 Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14, 583-594.
91. Sory, M. P., Boland, A., Lambermont, I. & Cornelis, G. R. 1995 Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl Acad. Sci. USA 92, 11998-12002.
92. Starnbach, M. N. & Bevan, M. J. 1994 Cells infected with Yersinia present an epitope to class I MHC-restricted CTL. J. Immunol. 153, 1603-1612.
93. Tardy, F., Homblé, F., Neyt, C., Wattiez, R., Cornelis, G. R., Ruysschaert, J.-M. & Cabiaux, V. 1999 Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18, 6793-6799.
94. Uchiya, K., Barbieri, M. A., Funato, K., Shah, A. H., Stahl, P. D. & Groisman, E. A. 1999 A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18, 3924-3933.
95. Vallis, A. J., Finck-Barbançon, V., Yahr, T. L. & Frank, D. W. 1999 Biological effects of Pseudomonas aeruginosa type III-secreted proteins on CHO cells. Infect. Immun. 67, 2040-2044.
96. Van Gijsegem, F., Gough, C. L., Zischek, C., Niqueux, E., Arlat, M., Genin, S., Barberis, P., German, S., Castello, P. & Boucher, C. 1995 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.
97. Van Nhieu, G. T. & Sansonetti, P. J. 1999 Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2, 51-55.
98. Van Nhieu, G. T., BenZeev, A. & Sansonetti, P. J. 1997 Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J. 16, 2717-2729.
99. Van Nhieu, G. T., Caron, E., Hall, A. & Sansonetti, P. J. 1999 IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J. 18, 3249-3262.
100. Viprey, V., Del Greco, A., Golinowski, W., Broughton, W. J. & Perret, X. 1998 Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28, 1381-1389.
101. Wachter, C., Beinke, C., Mattes, M. & Schmidt, M. A. 1999 Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 31, 1695-1707.
102. Wainwright, L. A. & Kaper, J. B. 1998 EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol. Microbiol. 27, 1247-1260.
103. Watarai, M., Tobe, T., Yoshikawa, M. & Sasakawa, C. 1995 Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J. 14, 2461-2470.
104. Wattiau, P. & Cornelis, G. R. 1993 SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol. Microbiol. 8, 123-131.
105. Wattiau, P., Bernier, B., Deslee, P., Michiels, T. & Cornelis, G. R. 1994 Individual chaperones required for Yop secretion by Yersinia. Proc. Natl Acad. Sci. USA 91, 10493-10497.
106. Wattiau, P., Woestyn, S. & Cornelis, G. R. 1996 Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20, 255-262.
107. Woestyn, S., Allaoui, A., Wattiau, P. & Cornelis, G. R. 1994 YscN, the putative energizer of the Yersinia Yop secretion machinery. J. Bacteriol. 176, 1561-1569.
108. Woestyn, S., Sory, M. P., Boland, A., Lequenne, O. & Cornelis, G. R. 1996 The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes. Mol. Microbiol. 20, 1261-1271.
109. Wolff, C., Nisan, I., Hanski, E., Frankel, G. & Rosenshine, I. 1998 Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 28, 143-155.
110. Yahr, T. L., Vallis, A. J., Hancock, M. K., Barbieri, J. T. & Frank, D. W. 1998 ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl Acad. Sci. USA 95, 13899-13904.
111. Young, G. M., Schmiel, D. H. & Miller, V. L. 1999 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.
112. Zhou, D., Mooseker, M. S. & Galan, J. E. 1999 Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092-2095.
113. Zumbihl, R., Aepfelbacher, M., Andor, A., Jacobi, C. A., Ruckdeschel, H., Rouot, B. & Heesemann, J. 1999 The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small CTP-binding protein RhoA. J. Biol. Chem. 274, 29289-29293.