Process of protein transport by the type III secretion system

Microbiology and Molecular Biology Reviews

Volumn 68, Issue 4, 2004, Pages 771-795

  Ghosh, Partho ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN; CHAPERONE; MESSENGER RNA; SECRETIN;

AMINO ACID SEQUENCE; BACTERIAL FLAGELLUM; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERIUM PILUS; CHEMICAL ANALYSIS; CYTOSOL; EFFECTOR CELL; GENETIC TRANSFECTION; GRAM NEGATIVE BACTERIUM; HOST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; RNA SEQUENCE; SIGNAL TRANSDUCTION; STOICHIOMETRY;

BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; MOLECULAR CHAPERONES; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 10344249890     PISSN: 10922172     EISSN: None     Source Type: Journal    
DOI: 10.1128/MMBR.68.4.771-795.2004     Document Type: Review

References (257)

1. Abe, A., M. de Grado, R. A. Pfuetzner, C. Sánchez- Sanmartín, R. Devinney, J. L. Puente, N. C. Strynadka, and B. B. Finlay. 1999. Enteropathogenic Escherichia coli translocated intimin receptor, Tir, requires a specific chaperone for stable secretion. Mol. Microbiol. 33:1162-1175.
2. Aizawa, S. I. 2001. Bacterial flagella and type III secretion systems. FEMS Microbiol. Lett. 202:157-164.
3. Albright, R. A., M. C. Mossing, and B. W. Matthews. 1996. High-resolution structure of an engineered Cro monomer shows changes in conformation relative to the native dimer. Biochemistry 35:735-742.
4. Allaoui, A., S. Woestyn, C. Sluiters, and G. R. Cornelis. 1994. YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J. Bacteriol. 176:4534-4542.
5. Anderson, D. M., D. E. Fouts, A. Collmer, and O. Schneewind. 1999. Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals. Proc. Natl. Acad. Sci. USA 96:12839-12843.
6. Anderson, D. M., K. S. Ramamurthi, C. Tam, and O. Schneewind. 2002. YopD and LcrH regulate expression of Yersinia enterocolitica YopQ by a posttranscriptional mechanism and bind to yopQ RNA. J. Bacteriol. 184:1287-1295.
7. Anderson, D. M., and O. Schneewind. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-1143.
8. Anderson, D. M., and O. Schneewind. 1999. Type III machines of Gram-negative pathogens: injecting virulence factors into host cells and more. Curr. Opin. Microbiol. 2:18-24.
9. Anderson, D. M., and O. Schneewind. 1999. Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol. Microbiol. 31:1139-1148.
10. Anderson, W. F., D. H. Ohlendorf, Y. Takeda, and B. W. Matthews. 1981. Structure of the cro repressor from bacteriophage lambda and its interaction with DNA. Nature 290:754-758.
11. Andersson, K., K. E. Magnusson, M. Majeed, O. Stendahl, and M. Fallman. 1999. Yersinia pseudotuberculosis-induced calcium signaling in neutrophils is blocked by the virulence effector YopH. Infect. Immun. 67:2567-2574.
12. Auvray, F., A. J. Ozin, L. Claret, and C. Hughes. 2002. Intrinsic membrane targeting of the flagellar export ATPase Flil: interaction with acidic phospholipids and FliH. J. Mol. Biol. 318:941-950.
13. Bennett, M. J., S. Choe, and D. Eisenberg. 1994. Domain swapping: entangling alliances between proteins. Proc. Natl. Acad. Sci. USA 91:3127-3131.
14. Bergman, T., K. Erickson, E. Galyov, C. Persson, and H. Wolf-Watz. 1994. The IcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J. Bacteriol. 176:2619-2626.
15. Birtalan, S., and P. Ghosh. 2001. Structure of the Yersinia type III secretory system chaperone SycE. Nat. Struct. Biol. 8:974-978.
16. Birtalan, S. C., R. M. Phillips, and P. Ghosh. 2002. Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol. Cell 9:971-980.
17. Black, D. S., L. G. Montagna, S. Zitsmann, and J. B. Bliska. 1998. Identification of an amino-terminal substrate-binding domain in the Yersinia tyrosine phosphatase that is required for efficient recognition of focal adhesion targets. Mol. Microbiol. 29:1263-1274.
18. Bleves, S., M. N. Marenne, G. Detry, and G. R. Cornelis. 2002. Up-regulation of the Yersinia enterocolitica yop regulon by deletion of the flagellum master operon flhDC. J. Bacteriol. 184:3214-3223.
19. Blocker, A., N. Jouihri, E. Larquet, P. Gounon, F. Ebel, C. Parsot, P. Sansonetti, and A. Allaoui. 2001. Structure and composition of the Shigella flexneri "needle complex," a part of its type III secreton. Mol. Microbiol. 39:652-663.
20. Blocker, A., K. Komoriya, and S. Aizawa. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100:3027-3030.
21. Bogdanove, A. J., Z. M. Wei, L. Zhao, and S. V. Beer. 1996. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J. Bacteriol. 178:1720-1730.
22. Boland, A., M. P. Sory, M. Iriarte, C. Kerbourch, P. Wattiau, and G. R. Cornelis. 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.
23. Boyd, A. P., I. Lambermont, and G. R. Cornelis. 2000. 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.
24. Bronstein, P. A., E. A. Miao, and S. I. Miller. 2000. InvB is a type III secretion chaperone specific for SspA. J. Bacteriol. 182:6638-6644.
25. Burghout, P., R. Van Boxtel, P. Van Gelder, P. Ringler, S. A. Muller, J. Tommassen, and M. Koster. 2004. Structure and electrophysiological properties of the YscC secretin from the type III secretion system of Yersinia enterocolitica. J. Bacteriol. 186:4645-4654.
26. Burr, S. E., K. Stuber, T. Wahli, and J. Frey. 2002. Evidence for a type III secretion system in Aeromonas salmonicida subsp. salmonicida. J. Bacteriol. 184:5966-5970.
27. Cambronne, E. D., L. W. Cheng, and O. Schneewind. 2000. LcrQ/YscM1, regulators of the Yersinia yop virulon, are injected into host cells by a chaperone-dependent mechanism. Mol. Microbiol. 37:263-273.
28. Cambronne, E. D., and O. Schneewind. 2002. Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5′ untranslated region of yop mRNA. J. Bacteriol. 184:5880-5893.
29. Cambronne, E. D., J. A. Sorg, and O. Schneewind. 2004. Binding of SycH chaperone to YscM1 and YscM2 activates effector yop expression in Yersinia enterocolitica. J. Bacteriol. 186:829-841.
30. Charkowski, A. O., H. C. Huang, and A. Collmer. 1997. Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membranes of gram-negative bacteria. J. Bacteriol. 179:3866-3874.
31. Cheng, L. W., D. M. Anderson, and O. Schneewind. 1997. Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol. Microbiol. 24:757-765.
32. Cheng, L. W., and O. Schneewind. 1999. Yersinia enterocolitica type III secretion. On the role of SycE in targeting YopE into HeLa cells. J. Biol. Chem. 274:22102-22108.
33. Claret, L., S. R. Calder, M. Higgins, and C. Hughes. 2003. Oligomerization and activation of the Flil ATPase central to bacterial flagellum assembly. Mol. Microbiol. 48:1349-1355.
34. Cordes, F. S., K. Komoriya, E. Larquet, S. Yang, E. H. Egelman, A. Blocker, and S. M. Lea. 2003. Helical structure of the needle of the type III secretion system of Shigella flexneri. J. Biol. Chem. 278:17103-17107.
35. Cornelis, G., J. C. Vanootegem, and C. Sluiters. 1987. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb. Pathog. 2:367-379.
36. Cornelis, G. R. 1998. The Yersinia deadly kiss. J. Bacteriol. 180:5495-5504.
37. Cornelis, G. R. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-408.
38. Cornelis, G. R. 2002. The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell. Biol. 3:742-752.
39. Cornelis, G. R., A. Boland, A. P. Boyd, C. Geuijen, M. Iriarte, C. Neyt, M. P. Sory, and I. Stainier. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62:1315-1352.
40. Cornelis, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
41. Crago, A. M., and V. Koronakis. 1998. Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol. Microbiol. 30:47-56.
42. Creasey, E. A., R. M. Delahay, A. A. Bishop, R. K. Shaw, B. Kenny, S. Knutton, and G. Frankel. 2003. CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol. Microbiol. 47:209-221.
43. Creasey, E. A., R. M. Delahay, S. J. Daniell, and G. Frankel. 2003. Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 149:2093-2106.
44. Crestfield, A. M., W. H. Stein, and S. Moore. 1962. On the aggregation of bovine pancreatic ribonuclease. Arch. Biochem. Biophys. Suppl. 1:217-222.
45. Dale, C., G. R. Plague, B. Wang, H. Ochman, and N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA 99:12397-12402.
46. Dale, C., S. A. Young, D. T. Haydon, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98:1883-1888.
47. Daniell, S. J., E. Kocsis, E. Morris, S. Knutton, F. P. Booy, and G. Frankel. 2003. 3D structure of EspA filaments from enteropathogenic Escherichia coli. Mol. Microbiol. 49:301-308.
48. Daniell, S. J., N. Takahashi, R. Wilson, D. Friedberg, I. Rosenshine, F. P. Booy, R. K. Shaw, S. Knutton, G. Frankel, and S. Aizawa. 2001. The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell. Microbiol. 3:865-871.
49. Darwin, K. H., and V. L. Miller. 2000. The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes. Mol. Microbiol. 35:949-960.
50. Darwin, K. H., and V. L. Miller. 2001. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J. 20:1850-1862.
51. Daughdrill, G. W., M. S. Chadsey, J. E. Karlinsey, K. T. Hughes, and F. W. Dahlquist. 1997. The C-terminal half of the anti-sigma factor, FIgM, becomes structured when bound to its target, sigma 28. Nat. Struct. Biol. 4:285-291.
52. Day, J. B., F. Ferracci, and G. V. Plano. 2003. Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies. Mol. Microbiol. 47:807-823.
53. Day, J. B., I. Guller, and G. V. Plano. 2000. Yersinia pestis YscG protein is a Syc-like chaperone that directly binds yscE. Infect. Immun. 68:6466-6471.
54. Day, J. B., and G. V. Plano. 1998. A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol. Microbiol. 30:777-788.
55. Deleuil, F., L. Mogemark, M. S. Francis, H. Wolf-Watz, and M. Fallman. 2003. Interaction between the Yersinia protein tyrosine phosphatase YopH and eukaryotic Cas/Fyb is an important virulence mechanism. Cell. Microbiol. 5:53-64.
56. Di Genaro, M. S., M. Waidmann, U. Kramer, N. Hitziger, E. Bohn, and I. B. Autenrieth. 2003. Attenuated Yersinia enterocolitica mutant strains exhibit differential virulence in cytokine-deficient mice: implications for the development of novel live carrier vaccines. Infect. Immun. 71:1804-1812.
57. Doolittle, R. F. 1981. Similar amino acid sequences: chance or common ancestry? Science 214:149-159.
58. Driks, A., and D. J. DeRosier. 1990. Additional structures associated with bacterial flagellar basal body. J. Mol. Biol. 211:669-672.
59. Ebel, F., T. Podzadel, M. Ronde, A. U. Kresse, S. Kramer, C. Deibel, C. A. Guzman, and T. Chakraborty. 1998. Initial binding of Shiga toxin-producing Escherichia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol. Microbiol. 30:147-161.
60. Edqvist, P. J., J. Olsson, M. Lavander, L. Sundberg, A. Forsberg, H. Wolf-Watz, and S. A. Lloyd. 2003. YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J. Bacteriol. 185:2259-2266.
61. Ehrbar, K., A. Friebel, S. I. Miller, and W. D. Hardt. 2003. Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J. Bacteriol. 185:6950-6967.
62. Ehrbar, K., S. Hapfelmeier, B. Stecher, and W. D. Hardt. 2004. InvB is required for type III-dependent secretion of SopA in Salmonella enterica serovar Typhimurium. J. Bacteriol. 186:1215-1219.
63. 1 ATPase family of proteins. J. Bacteriol. 176:4501-4510.
64. Elliott, S. J., S. W. Hutcheson, M. S. Dubois, J. L. Mellies, L. A. Wainwright, M. Batchelor, G. Frankel, S. Knutton, and J. B. Kaper. 1999. Identification of CesT a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol. Microbiol. 33:1176-1189.
65. Emerson, S. U., K. Tokuyasu, and M. I. Simon. 1970. Bacterial flagella: polarity of elongation. Science 169:190-192.
66. Evdokimov, A. G., D. E. Anderson, K. M. Routzahn, and D. S. Waugh. 2001. Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J. Mol. Biol. 312:807-821.
67. Evdokimov, A. G., J. Phan, J. E. Tropea, K. M. Routzahn, H. K. Peters, M. Pokross, and D. S. Waugh. 2003. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat. Struct. Biol. 10:789-793.
68. Evdokimov, A. G., J. E. Tropea, K. M. Routzahn, T. D. Copeland, and D. S. Waugh. 2001. Structure of the N-terminal domain of Yersinia pestis YopH at 2.0 Å resolution. Acta Crystallogr. Sect. D 57:793-799.
69. Evdokimov, A. G., J. E. Tropea, K. M. Routzahn, and D. S. Waugh. 2002. Crystal structure of the Yersinia pestis GTPase activator YopE. Protein Sci. 11:401-408.
70. Evdokimov, A. G., J. E. Tropea, K. M. Routzahn, and D. S. Waugh. 2002. Three-dimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr. Sect. D 58:398-406.
71. Fadouloglou, V. E., A. P. Tampakaki, N. M. Glykos, M. N. Bastaki, J. M. Hadden, S. E. Phillips, N. J. Panopoulos, and M. Kokkinidis. 2004. Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems. Proc. Natl. Acad. Sci. USA 101:70-75.
72. Fan, F., K. Ohnishi, N. R. Francis, and R. M. Macnab. 1997. The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol. Microbiol. 26:1035-1046.
73. Feldman, M. F., S. Muller, E. Wuest, and G. R. Cornelis. 2002. SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol. Microbiol. 46:1183-1197.
74. Fenselau, S., I. Balbo, and U. Bonas. 1992. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant-Microbe Interact. 5:390-396.
75. Ffrench-Constant, R. H., N. Waterfield, V. Burland, N. T. Perna, P. J. Daborn, D. Bowen, and F. R. Blattner. 2000. A genomic sample sequence of the entomopathogenic bacterium Photorhabdus luminescens W14: potential implications for virulence. Appl. Environ. Microbiol. 66:3310-3329.
76. 2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J. Bacteriol. 176:569-579.
77. Finck-Barbançon, V., T. L. Yahr, and D. W. Frank. 1998. Identification and characterization of SpcU, a chaperone required for efficient secretion of the ExoU cytotoxin. J. Bacteriol. 180:6224-6231.
78. Forsberg, A., and H. Wolf-Watz. 1990. Genetic analysis of the yopE region of Yersinia spp.: identification of a novel conserved locus, yerA, regulating yopE expression. J. Bacteriol. 172:1547-1555.
79. Forsberg, A., and H. Wolf-Watz. 1988. The virulence protein Yop5 of Yersinia pseudotuberculosis is regulated at transcriptional level by plasmid-plB1-encoded trans-acting elements controlled by temperature and calcium. Mol. Microbiol. 2:121-133.
80. Foultier, B., P. Troisfontaines, D. Vertommen, M. N. Marenne, M. Rider, C. Parsot, and G. R. Cornelis. 2003. Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system. Infect. Immun. 71:242-253.
81. Francis, M. S., S. A. Lloyd, and H. Wolf-Watz. 2001. The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthesis in Yersinia pseudotuberculosis. Mol. Microbiol. 42:1075-1093.
82. Francis, M. S., and H. Wolf-Watz. 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.
83. Francis, M. S., H. Wolf-Watz, and A. Forsberg. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-172.
84. Frank, D. W. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26:621-629.
85. Fraser, G. M., B. Gonzalez-Pedrajo, J. R. Tame, and R. M. Macnab. 2003. Interactions of FliJ with the Salmonella type III flagellar export apparatus. J. Bacteriol. 185:5546-5554.
86. Fraser, G. M., T. Hirano, H. U. Ferris, L. L. Devgan, M. Kihara, and R. M. Macnab. 2003. Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol. Microbiol. 48:1043-1057.
87. Frithz-Lindsten, E., R. Rosqvist, L. Johansson, and A. Forsberg. 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.
88. Galán, J. E. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53-86.
89. Galán, J. E., and A. Collmer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
90. Galán, J. E., C. Ginocchio, and P. Costeas. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J. Bacteriol. 174:4338-4349.
91. Gauthier, A., and B. B. Finlay. 2003. Translocated intimin receptor and its chaperone interact with ATPase of the type III secretion apparatus of enteropathogenic Escherichia coli. J. Bacteriol. 185:6747-6755.
92. Genin, S., and C. A. Boucher. 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.
93. Ginocchio, C. C., and J. E. Galan. 1995. Functional conservation among members of the Salmonella typhimurium InvA family of proteins. Infect. Immun. 63:729-732.
94. Ginocchio, C. C., S. B. Olmsted, C. L. Wells, and J. E. Galan. 1994. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76:717-724.
95. 1-ATPase. Nature 409:637-641.
96. Gophna, U., E. Z. Ron, and D. Graur. 2003. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151-163.
97. Gotte, G., M. Bertoldi, and M. Libonati. 1999. Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme. Eur. J. Biochem. 265:680-687.
98. Graumann, J., H. Lilie, X. Tang, K. A. Tucker, J. H. Hoffmann, J. Vijayalakshmi, M. Saper, J. C. Bardwell, and U. Jakob. 2001. Activation of the redox-regulated molecular chaperone Hsp33 - a two-step mechanism. Structure 9:377-387.
99. Griffin, B. A., S. R. Adams, J. Jones, and R. Y. Tsien. 2000. Fluorescent labeling of recombinant proteins in living cells with FIAsH. Methods Enzymol. 327:565-578.
100. Guttman, D. S., B. A. Vinatzer, S. F. Sarkar, M. V. Ranall, G. Kettler, and J. T. Greenberg. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-1726.
101. Hakansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 1996. 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.
102. Hale, T. L., E. V. Oaks, and S. B. Formal. 1985. Identification and antigenic characterization of virulence-associated, plasmid-coded proteins of Shigella spp. and enteroinvasive Escherichia coli. Infect. Immun. 50:620-629.
103. Haller, J. C., S. Carlson, K. J. Pederson, and D. E. Pierson. 2000. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence. Mol. Microbiol. 36:1436-1446.
104. Hartland, E. L., S. J. Daniell, R. M. Delahay, B. C. Neves, T. Wallis, R. K. Shaw, C. Hale, S. Knutton, and G. Frankel. 2000. The type III protein translocation system of enteropathogenic Escherichia coli involves EspA-EspB protein interactions. Mol. Microbiol. 35:1483-1492.
105. Hayward, R. D., E. J. McGhie, and V. Koronakis. 2000. Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion. Mol. Microbiol. 37:727-739.
106. Hensel, M., J. E. Shea, S. R. Waterman, R. Mundy, T. Nikolaus, G. Banks, A. Vazquez-Torres, C. Gleeson, F. C. Fang, and D. W. Holden. 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.
107. Hoiczyk, E., and G. Blobel. 2001. Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc. Natl. Acad. Sci. USA 98:4669-4674.
108. Hsia, R. C., Y. Pannekoek, E. Ingerowski, and P. M. Bavoil. 1997. Type III secretion genes identify a putative virulence locus of Chlamydia. Mol. Microbiol. 25:351-359.
109. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
110. Hume, P. J., E. J. McGhie, R. D. Havward, and V. Koronakis. 2003. The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol. Microbiol. 49:425-439.
111. Ide, T., S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M. A. Schmidt. 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell. Microbiol. 3:669-679.
112. Iino, T. 1969. Polarity of flagellar growth in Salmonella. J. Gen. Microbiol. 56:227-239.
113. Iriarte, M., and G. R. Cornelis. 1998. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29:915-929.
114. Jackson, M. W., and G. V. Plano. 2000. Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol. Lett. 186:85-90.
115. Jacobi, C. A., A. Roggenkamp, A. Rakin, R. Zumbihl, L. Leitritz, and J. Heesemann. 1998. In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene. Mol. Microbiol. 30:865-882.
116. Jarvis, K. G., J. A. Gíron, A. E. Jerse, T. K. McDaniel, M. S. Donnenberg, and J. B. Kaper. 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.
117. Jin, Q., and S.-Y. He. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-2558.
118. Jones, C. J., R. M. Macnab, H. Okino, and S. Aizawa. 1990. Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J. Mol. Biol. 212:377-387.
119. Jouihri, N., M. P. Sory, A. L. Page, P. Gounon, C. Parsot, and A. Allaoui. 2003. 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.
120. Journet, L., C. Agrain, P. Broz, and G. R. Cornelis. 2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302:1757-1760.
121. Khandelwal, P., K. Keliikuli, C. L. Smith, M. A. Saper, and E. R. Zuiderweg. 2002. Solution structure and phosphopeptide binding to the N-terminal domain of Yersinia YopH: comparison with a crystal structure. Biochemistry 41:11425-11437.
122. Kihara, M., T. Minamino, S. Yamaguchi, and R. M. Macnab. 2001. Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J. Bacteriol. 183:1655-1662.
123. Kimbrough, T. G., and S. I. Miller. 2000. Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc. Natl. Acad. Sci. USA 97:11008-11013.
124. Knutton, S., I. Rosenshine, M. J. Pallen, I. Nisan, B. C. Neves, C. Bain, C. Wolff, G. Dougan, and G. Frankel. 1998. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17:2166-2176.
125. Koster, M., W. Bitter, H. de Cock, A. Allaoui, G. R. Cornelis, and J. Tommassen. 1997. The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol. Microbiol. 26:789-797.
126. Krall, R., Y. Zhang, and J. T. Barbieri. 2004. Intracellular membrane localization of Pseudomonas ExoS and Yersinia YopE in mammalian cells. J. Biol. Chem. 279:2747-2753.
127. Kraulis, P. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of proteins. J. Appl. Crystallogr. 24:946-950.
128. Kubori, T., and J. E. Galan. 2002. Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J. Bacteriol. 184:4699-4708.
129. Kubori, T., and J. E. Galan. 2003. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115:333-342.
130. Kubori, T., Y. Matsushima, D. Nakamura, J. Uralil, M. Lara-Tejero, A. Sukhan, J. E. Galán, and S. I. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602-605.
131. Kubori, T., A. Sukhan, S. I. Aizawa, and J. E. Galan. 2000. 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.
132. Lacy, E. R., I. Filippov, W. S. Lewis, S. Otieno, L. Xiao, S. Weiss, L. Hengst, and R. W. Kriwacki. 2004. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol. 11:358-364.
133. Lavander, M., L. Sundberg, P. J. Edqvist, S. A. Lloyd, H. Wolf-Watz, and A. Forsberg. 2002. Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J. Bacteriol. 184:4500-4509.
134. Lee, S. H., and J. E. Galan. 2003. InvB is a type III secretion-associated chaperone for the Salmonella enterica effector protein SopE. J. Bacteriol. 185:7279-7284.
135. Lee, S. H., and J. E. Galan. 2004. Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51:483-495.
136. Lee, V. T., D. M. Anderson, and O. Schneewind. 1998. Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone. Mol. Microbiol. 28:593-601.
137. Lee, V. T., and O. Schneewind. 2002. Yop fusions to tightly folded protein domains and their effects on Yersinia enterocolitica type III secretion. J. Bacteriol. 184:3740-3745.
138. Li, C. M., I. Brown, J. Mansfield, C. Stevens, T. Boureau, M. Romantschuk, and S. Taira. 2002. 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.
139. Linderoth, N. A., M. N. Simon, and M. Russel. 1997. The filamentous phage pIV multimer visualized by scanning transmission electron microscopy. Science 278:1635-1638.
140. Liu, Y., and D. Eisenberg. 2002. 3D domain swapping: as domains continue to swap. Protein Sci. 11:1285-1299.
141. Lloyd, S. A., A. Forsberg, H. Wolf-Watz, and M. S. Francis. 2001. Targeting exported substrates to the Yersinia TTSS: different functions for different signals? Trends Microbiol. 9:367-371.
142. Lloyd, S. A., M. Norman, R. Rosqvist, and H. Wolf-Watz. 2001. Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol. Microbiol. 39:520-531.
143. Lloyd, S. A., M. Sjostrom, S. Andersson, and H. Wolf-Watz. 2002. Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol. Microbiol. 43:51-59.
144. Luo, Y., M. G. Bertero, E. A. Frey, R. A. Pfuetzner, M. R. Wenk, L. Creagh, S. L. Marcus, D. Lim, F. Sicheri, C. Kay, C. Haynes, B. B. Finlay, and N. C. Strynadka. 2001. Structural and biochemical characterization of the the type III secretion chaperones CesT and SigE. Nat. Struct. Biol. 8:1031-1036.
145. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
146. Magdalena, J., A. Hachani, M. Chamekh, N. Jouihri, P. Gounon, A. Blocker, and A. Allaoui. 2002. Spa32 regulates a switch in substrate specificity of the type III secretion of Shigella flexneri from needle components to Ipa proteins. J. Bacteriol. 184:3433-3441.
147. Makino, K., K. Oshima, K. Kurokawa, K. Yokoyama, T. Uda, K. Tagomori, Y. Iijima, M. Najima, M. Nakano, A. Yamashita, Y. Kubota, S. Kimura, T. Yasunaga, T. Honda, H. Shinagawa, M. Hattori, and T. Iida. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet 361:743-749.
148. Marenne, M. N., L. Journet, L. J. Mota, and G. R. Cornelis. 2003. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb. Pathog. 35:243-258.
149. Mavris, M., A. L. Page, R. Tournebize, B. Demers, P. Sansonetti, and C. Parsot. 2002. Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol. Microbiol. 43:1543-1553.
150. McDaniel, T. K., K. G. Jarvis, M. S. Donnenberg, and J. B. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92:1664-1668.
151. McGhie, E. J., P. J. Hume, R. D. Hayward, J. Torres, and V. Koronakis. 2002. Topology of the Salmonella invasion protein SipB in a model bilayer. Mol. Microbiol. 44:1309-1321.
152. Melen, K., A. Krogh, and G. von Heijne. 2003. Reliability measures for membrane protein topology prediction algorithms. J. Mol. Biol. 327:735-744.
153. Michiels, T., J. C. Vanooteghem, C. Lambert de Rouvroit, B. China, A. Gustin, P. Boudry, and G. R. Cornelis. 1991. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J. Bacteriol. 173:4994-5009.
154. Michiels, T., P. Wattiau, R. Brasseur, J. M. Ruysschaert, and G. Cornelis. 1990. Secretion of Yop proteins by yersiniae. Infect. Immun. 58:2840-2849.
155. Minamino, T., B. Gonzalez-Pedrajo, M. Kihara, K. Namba, and R. M. Macnab. 2003. The ATPase Flil can interact with the type III flagellar protein export apparatus in the absence of its regulator. FliH. J. Bacteriol. 185:3983-3988.
156. Minamino, T., and R. M. Macnab. 2000. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 182:4906-4914.
157. Minamino, T., and R. M. MacNab. 2000. FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with Flil and inhibits its ATPase activity. Mol. Microbiol. 37:1494-1503.
158. Minamino, T., and R. M. MacNab. 2000. Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol. Microbiol. 35:1052-1064.
159. Montagna, L. G., M. I. Ivanov, and J. B. Bliska. 2001. Identification of
160. Mudgett, M. B., O. Chesnokova, D. Dahlbeck, E. T. Clark, O. Rossier, U. Bonas, and B. J. Staskawicz. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. USA 97:13324-13329.
161. Muramoto, K., S. Makishima, S. I. Aizawa, and R. M. Macnab. 1998. Effect of cellular level of FliK on flagellar hook and filament assembly in Salmonella typhimurium. J. Mol. Biol. 277:871-882.
162. Newcomer, M. E. 2002. Protein folding and three-dimensional domain swapping: a strained relationship? Curr. Opin. Struct. Biol. 12:48-53.
163. Neyt, C., and G. R. Cornelis. 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.
164. Neyt, C., and G. R. Cornelis. 1999. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol. Microbiol. 31:143-156.
165. Nguyen, L., I. T. Paulsen, J. Tchieu, C. J. Hueck, and M. H. Saier, Jr. 2000. Phylogenetic analyses of the constituents of type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2:125-144.
166. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
167. Nordfelth, R., and H. Wolf-Watz. 2001. YopB of Yersinia enterocolitica is essential for YopE translocation. Infect. Immun. 69:3516-3518.
168. Nouwen, N., N. Ranson, H. Saibil, B. Wolpensinger, A. Engel, A. Ghazi, and A. P. Pugsley. 1999. Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proc. Natl. Acad. Sci. USA 96:8173-8177.
169. Nouwen, N., H. Stahlberg, A. P. Pugsley, and A. Engel. 2000. Domain structure of secretin PulD revealed by limited proteolysis and electron microscopy. EMBO J. 19:2229-2236.
170. Opalka, N., R. Beckmann, N. Boisset, M. N. Simon, M. Russel, and S. A. Darst. 2003. Structure of the filamentous phage pIV multimer by cryoelectron microscopy. J. Mol. Biol. 325:461-470.
171. Page, A. L., P. Sansonetti, and C. Parsot. 2002. Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol. Microbiol. 43:1533-1542.
172. Pallen, M. J., M. S. Francis, and K. Futterer. 2003. Tetratricopeptide- like repeats in type-III-secretion chaperones and regulators. FEMS Microbiol. Lett. 223:53-60.
173. Park, C., and R. T. Raines. 2000. Dimer formation by a "monomeric" protein. Protein Sci. 9:2026-2033.
174. Parsot, C., C. Hamiaux, and A. L. Page. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14.
175. Parsot, C., R. Menard, P. Gounon, and P. J. Sansonetti. 1995. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol. Microbiol. 16:291-300.
176. Payne, P. L., and S. C. Straley. 1998. YscO of Yersinia pestis is a mobile core component of the Yop secretion system. J. Bacteriol. 180:3882-3890.
177. Payne, P. L., and S. C. Straley. 1999. YscP of Yersinia pestis is a secreted component of the Yop secretion system. J. Bacteriol. 181:2852-2862.
178. Pederson, K. J., R. Krall, M. J. Riese, and J. T. Barbieri. 2002. Intracellular localization modulates targeting of ExoS, a type III cytotoxin, to eukaryotic signalling proteins. Mol. Microbiol. 46:1381-1390.
179. Pettersson, J., R. Nordfelth, E. Dubinina, T. Bergman, M. Gustafsson, K. E. Magnusson, and H. Wolf-Watz. 1996. Modulation of virulence factor expression by pathogen target cell contact. Science 273:1231-1233.
180. 2 inhibitors. J. Biol. Chem. 278:41326-41332.
181. Plano, G. V., S. S. Barve, and S. C. Straley. 1991. LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J. Bacteriol. 173:7293-7303.
182. Plano, G. V., J. B. Day, and F. Ferracci. 2001. Type III export: new uses for an old pathway. Mol. Microbiol. 40:284-293.
183. Plano, G. V., and S. C. Straley. 1995. Mutations in yscC, yscD, and yscG prevent high-level expression and secretion of V antigen and Yops in Yersinia, pestis. J. Bacteriol. 177:3843-3854.
184. Portnoy, D. A., H. Wolf-Watz, I. Bolin, A. B. Beeder, and S. Falkow. 1984. Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect. Immun. 43:108-114.
185. Pozidis, C., A. Chalkiadaki, A. Gomez-Serrano, H. Stahlberg, I. Brown, A. P. Tampakaki, A. Lustig, G. Sianidis, A. S. Politou, A. Engel, N. J. Panopoulos, J. Mansfield, A. P. Pugsley, S. Karamanou, and A. Economou. 2003. Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. J. Biol. Chem. 278:25816-25824.
186. Preston, G., H. C. Huang, S. Y. He, and A. Collmer. 1995. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol. Plant-Microbe Interact. 8:717-732.
187. Ramamurthi, K. S., and O. Schneewind. 2002. Type III protein secretion in yersinia species. Annu. Rev. Cell Dev. Biol. 18:107-133.
188. Ramamurthi, K. S., and O. Schneewind. 2002. Yersinia enterocolitica type III secretion: mutational analysis of the yopQ secretion signal. J. Bacteriol. 184:3321-3328.
189. Ramamurthi, K. S., and O. Schneewind. 2003. Yersinia yopQ mRNA encodes a bipartite type III secretion signal in the first 15 codons. Mol. Microbiol. 50:1189-1198.
190. Reid, B. G., and G. C. Flynn. 1997. Chromophore formation in green fluorescent protein. Biochemistry 36:6786-6791.
191. Roine, E., J. Saarinen, N. Kalkkinen, and M. Romantschuk. 1997. Purified HrpA of Pseudomonas syringae pv. tomato DC3000 reassembles into pili. FEBS Lett. 417:168-172.
192. Roine, E., W. Wei, J. Yuan, E. L. Nurmiaho-Lassila, N. Kalkkinen, M. Romantschuk, and S. Y. He. 1997. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 94:3459-3464.
193. Rosqvist, R., A. Forsberg, M. Rimpileainen, T. Bergman, and H. Wolf-Watz. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4:657-667.
194. Rosqvist, R., A. Forsberg, and H. Wolf-Watz. 1991. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect. Immun. 59:4562-4569.
195. Rosqvist, R., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1995. Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J. 14:4187-4195.
196. Rosqvist, R., K. E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
197. Rossier, O., K. Wengelnik, K. Hahn, and U. Bonas. 1999. The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. Proc. Natl. Acad. Sci. USA 96:9368-9373.
198. Rousseau, F., J. W. Schymkowitz, and L. S. Itzhaki. 2003. The unfolding story of three-dimensional domain swapping. Structure 11:243-251.
199. suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl. Acad. Sci. USA 98:5596-5601.
200. Russmann, H., T. Kubori, J. Sauer, and J. E. Galan. 2002. Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol. Microbiol. 46:769-779.
201. Russo, A. A., P. D. Jeffrey, A. K. Patten, J. Massague, and N. P. Pavletich. 1996. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382:325-331.
202. Saier, M. H., Jr. 2004. Evolution of the bacterial type III protein secretion systems. Trends Microbiol. 12:113-115.
203. Samatey, F. A., K. Imada, S. Nagashima, F. Vonderviszt, T. Kumasaka, M. Yamamoto, and K. Namba. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337.
204. Sansonetti, P. J., D. J. Kopecko, and S. B. Formal. 1982. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35:852-860.
205. Savvides, S. N., H. J. Yeo, M. R. Beck, F. Blaesing, R. Lurz, E. Lanka, R. Buhrdorf, W. Fischer, R. Haas, and G. Waksman. 2003. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:1969-1980.
206. Schesser, K., E. Frithz-Lindsten, and H. Wolf-Watz. 1996. Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J. Bacteriol. 178:7227-7233.
207. Schoehn, G., A. M. Di Guilmi, D. Lemaire, I. Attree, W. Weissenhorn, and A. Dessen. 2003. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J. 22:4957-4967.
208. Schoenhals, G. J., and R. M. Macnab. 1996. Physiological and biochemical analyses of FlgH, a lipoprotein forming the outer membrane L ring of the flagellar basal body of Salmonella typhimurium. J. Bacteriol. 178:4200-4207.
209. Schymkowitz, J. W., F. Rousseau, H. R. Wilkinson, A. Friedler, and L. S. Itzhaki. 2001. Observation of signal transduction in three-dimensional domain swapping. Nat. Struct. Biol. 8:888-892.
210. Sekiya, K., M. Ohishi, T. Ogino, K. Tamano, C. Sasakawa, and A. Abe. 2001. 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.
211. Shea, J. E., M. Hensel, C. Gleeson, and D. W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:2593-2597.
212. Smith, C. L., P. Khandelwal, K. Keliikuli, E. R. Zuiderweg, and M. A. Saper. 2001. Structure of the type III secretion and substrate-binding domain of Yersinia YopH phosphatase. Mol. Microbiol. 42:967-979.
213. Sory, M. P., A. Boland, I. Lambermont, and G. R. Cornelis. 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. Nat. Acad. Sci. USA 92:11998-12002.
214. Sory, M. P., and G. R. Cornelis. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
215. Stebbins, C. E., and J. E. Galan. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81.
216. Stebbins, C. E., and J. E. Galan. 2003. Priming virulence factors for delivery into the host. Nat. Rev. Mol. Cell. Biol. 4:738-743.
217. Stebbins, C. E., and J. E. Galán. 2000. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6:1449-1460.
218. Sukhan, A., T. Kubori, J. Wilson, and J. E. Galan. 2001. Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J. Bacteriol. 183:1159-1167.
219. Sundberg, L., and A. Forsberg. 2003. TyeA of Yersinia pseudotuberculosis is involved in regulation of Yop expression and is required for polarized translocation of Yop effectors. Cell. Microbiol. 5:187-202.
220. Suzuki, H., K. Yonekura, and K. Namba. 2004. Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J. Mol. Biol. 337:105-113.
221. Tamano, K., S. Aizawa, E. Katayama, T. Nonaka, S. Imajoh-Ohmi, A. Kuwae, S. Nagai, and C. Sasakawa. 2000. 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.
222. Tamano, K., E. Katayama, T. Toyotome, and C. Sasakawa. 2002. Shigella Spa32 is an essential secretory protein for functional type III secretion machinery and uniformity of its needle length. J. Bacteriol. 184:1244-1252.
223. Tardy, F., F. Homble, C. Neyt, R. Wattiez, G. R. Cornelis, J. M. Ruysschaert, and V. Cabiaux. 1999. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:6793-6799.
224. Tengel, T., I. Sethson, and M. S. Francis. 2002. Conformational analysis by CD and NMR spectroscopy of a peptide encompassing the amphipathic domain of YopD from Yersinia. Eur. J. Biochem. 269:3659-3668.
225. Thomas, J., G. P. Stafford, and C. Hughes. 2004. Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc. Natl. Acad. Sci. USA 101:3945-3950.
226. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
227. Topell, S., J. Hennecke, and R. Glockshuber. 1999. Circularly permuted variants of the green fluorescent protein. FEBS Lett. 457:283-289.
228. Touchette, N. A., K. M. Perry, and C. R. Matthews. 1986. Folding of dihydrofolate reductase from Escherichia coli. Biochemistry 25:5445-5452.
229. Trame, C. B., and D. B. McKay. 2003. Structure of the Yersinia enterocolitica molecular-chaperone protein SycE. Acta Crystallogr. Sect. D 59:389-392.
230. Trcek, J., G. Wilharm, C. A. Jacobi, and J. Heesemann. 2002. Yersinia enterocolitica YopQ: strain-dependent cytosolic accumulation and posttranslational secretion. Microbiology 148:1457-1465.
231. Trulzsch, K., A. Roggenkamp, M. Aepfelbacher, G. Wilharm, K. Ruckdeschel, and J. Heesemann. 2003. Analysis of chaperone-dependent Yop secretion/translocation and effector function using a mini-virulence plasmid of Yersinia enterocolitica. Int. J. Med. Microbiol. 293:167-177.
232. Tucker, S. C., and J. E. Galan. 2000. Complex function for SicA, a Salmonella enterica serovar Typhimurium type III secretion-associated chaperone. J. Bacteriol. 182:2262-2268.
233. Turner, L., W. S. Ryu, and H. C. Berg. 2000. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182:2793-2801.
234. Van Arnam, J. S., J. L. McMurry, M. Kihara, and R. M. Macnab. 2004. Analysis of an engineered Salmonella flagellar fusion protein, FliR-FlhB. J. Bacteriol. 186:2495-2498.
235. van Eerde, A., C. Hamiaux, J. Perez, C. Parsot, and B. W. Dijkstra. 2004. Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep. 5:477-483.
236. Van Gijsegem, F., C. Gough, C. Zischek, E. Niqueux, M. Arlat, S. Genin, P. Barberis, S. German, P. Castello, and C. Boucher. 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.
237. Van Gijsegem, F., J. Vasse, J. C. Camus, M. Marenda, and C. Boucher. 2000. Ralstonia solanacearum produces hrp-dependent pili that are required for PopA secretion but not for attachment of bacteria to plant cells. Mol. Microbiol. 36:249-260.
238. Vijayalakshmi, J., M. K. Mukhergee, J. Graumann, U. Jakob, and M. A. Saper. 2001. The 2.2 Å crystal structure of Hsp33: a heat shock protein with redox-regulated chaperone activity. Structure 9:367-375.
239. Wattiau, P., B. Bernier, P. Deslée, T. Michiels, and G. R. Cornelis. 1994. Individual chaperones required for Yop secretion by Yersinia. Proc. Nal. Acad. Sci. USA 91:10493-10497.
240. Wattiau, P., and G. R. Cornelis. 1993. SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol. Microbiol. 8:123-131.
241. Wilharm, G., V. Lehmann, K. Krauss, B. Lehnert, S. Richter, K. Ruckdeschel, J. Heesemann, and K. Trulzsch. 2004. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72:4004-4009.
242. Wilharm, G., W. Neumayer, and J. Heesemann. 2003. Recombinant Yersinia enterocolitica YscM1 and YscM2: homodimer formation and susceptibility to thrombin cleavage. Protein Expression Purif. 31:167-172.
243. Williams, A. W., and S. C. Straley. 1998. YopD of Yersinia pestis plays a role in negative regulation of the low-calcium response in addition to its role in translocation of Yops. J. Bacteriol. 180:350-358.
244. Wilson, R. K., R. K. Shaw, S. Daniell, S. Knutton, and G. Frankel. 2001. Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli. Cell. Microbiol. 3:753-762.
245. Woestyn, S., A. Allaoui, P. Wattiau, and G. R. Cornelis. 1994. YscN, the putative energizer of the Yersinia Yop secretion machinery. J. Bacteriol. 176:1561-1569.
246. Woestyn, S., M. P. Sory, A. Boland, O. Lequenne, and G. R. Cornelis. 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.
247. Wulff-Strobel, C. R., A. W. Williams, and S. C. Straley. 2002. 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.
248. Yahr, T. L., J. Goranson, and D. W. Frank. 1996. Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol. Microbiol. 22:991-1003.
249. Yeo, H. J., S. N. Savvides, A. B. Herr, E. Lanka, and G. Waksman. 2000. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 6:1461-1472.
250. Yonekura, K., S. Maki-Yonekura, and K. Namba. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-650.
251. Young, B. M., and G. M. Young. 2002. YpIA is exported by the Ysc, Ysa, and flagellar type III secretion systems of Yersinia enterocolitica. J. Bacteriol. 184:1324-1334.
252. Young, G. M., D. H. Schmiel, and V. L. Miller. 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.
253. Yuk, M. H., E. T. Harvill, and J. F. Miller. 1998. The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol. Microbiol. 28:945-959.
254. Zhang, Z. Y., J. C. Clemens, H. L. Schubert, J. A. Stuckey, M. W. Fischer, D. M. Hume, M. A. Saper, and J. E. Dixon. 1992. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267:23759-23766.
255. Zhao, R., C. D. Amsler, P. Matsumura, and S. Khan. 1996. FliG and FliM distribution in the Salmonella typhimurium cell and flagellar basal bodies. J. Bacteriol. 178:258-265.
256. Zhao, R., N. Pathak, H. Jaffe, T. S. Reese, and S. Khan. 1996. FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body. J. Mol. Biol. 261:195-208.
257. Zhu, K., B. Gonzalez-Pedrajo, and R. M. Macnab. 2002. Interactions among membrane and soluble components of the flagellar export apparatus of Salmonella. Biochemistry 41:9516-9524.