CesT is a multi-effector chaperone and recruitment factor required for the efficient type III secretion of both LEE- and non-LEE-encoded effectors of enteropathogenic Escherichia coli

Molecular Microbiology

Volumn 57, Issue 6, 2005, Pages 1762-1779

  Thomas, Nikhil A ^a   Deng, Wanyin ^a   Puente, Jose L ^a,b   Frey, Elizabeth A ^c   Yip, Calvin K ^c   Strynadka, Natalie C J ^c   Finlay, B Brett ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CYTOPLASM PROTEIN; PROTEIN MAP; PROTEIN TIR; UNCLASSIFIED DRUG;

ARTICLE; CYTOPLASM; ESCHERICHIA COLI; HOST CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; INTESTINE CELL; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PHOSPHOPROTEINS; RECEPTORS, CELL SURFACE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 25144508100     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04802.x     Document Type: Article

References (69)

1. Abe, A., de Grado, M., Pfuetzner, R.A., Sanchez-Sanmartin, C., Devinney, R., Puente, J.L., et al. (1999) Enteropathogenic Escherichia coli translocated intimin receptor, Tir, requires a specific chaperone for stable secretion. Mol Microbiol 33: 1162-1175.
2. Auvray, F., Ozin, A.J., Claret, L., and Hughes, C. (2002) Intrinsic membrane targeting of the flagellar export ATPase FliI: interaction with acidic phospholipids and FliH. J Mol Biol 318: 941-950.
3. Bennett, J.C., and Hughes, C. (2000) From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol 8: 202-204.
4. Birtalan, S., and Ghosh, P. (2001) Structure of the Yersinia type III secretory system chaperone SycE. Nat Struct Biol 8: 974-978.
5. Birtalan, S.C., Phillips, R.M., and Ghosh, P. (2002) Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell 9: 971-980.
6. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., et al. (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol 39: 652-663.
7. Bronstein, P.A., Miao, E.A., and Miller, S.I. (2000) InvB is a type III secretion chaperone specific for SspA. J Bacteriol 182: 6638-6644.
8. Campellone, K.G., Giese, A., Tipper, D.J., and Leong, J.M. (2002) A tyrosine-phosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol Microbiol 43: 1227-1241.
9. Campellone, K.G., Robbins, D., and Leong, J.M. (2004) EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7: 217-228.
10. Charpentier, X., and Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
11. Cheng, L.W., and Schneewind, O. (1999) Yersinia enterocolitica type III secretion. On the role of SycE in targeting YopE into HeLa cells. J Biol Chem 274: 22102-22108.
12. Cheng, L.W., Anderson, D.M., and Schneewind, O. (1997) Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol Microbiol 24: 757-765.
13. Crawford, J.A., and Kaper, J.B. (2002) The N-terminus of enteropathogenic Escherichia coli (EPEC) Tir mediates transport across bacterial and eukaryotic cell membranes. Mol Microbiol 46: 855-868.
14. Creasey, E.A., Friedberg, D., Shaw, R.K., Umanski, T., Knutton, S., Rosenshine, I., and Frankel, G. (2003a) CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology 149: 3639-3647.
15. Creasey, E.A., Delahay, R.M., Bishop, A.A., Shaw, R.K., Kenny, B., Knutton, S., and Frankel, G. (2003b) CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol Microbiol 47: 209-221.
16. Delahay, R.M., Shaw, R.K., Elliott, S.J., Kaper, J.B., Knutton, S., and Frankel, G. (2002) Functional analysis of the enteropathogenic Escherichia coli type III secretion system chaperone CesT identifies domains that mediate substrate interactions. Mol Microbiol 43: 61-73.
17. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., et al. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
18. Deng, W., Li, Y., Hardwidge, P.R., Frey, E.A., Pfuetzner, R.A., Lee, S., et al. (2005) Regulation of type III secretion system hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 73: 2135-2146.
19. van Eerde, A., Hamiaux, C., Perez, J., Parsot, C., and Dijkstra, B.W. (2004) Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep 5: 477-483.
20. Ehrbar, K., Friebel, A., Miller, S.I., and Hardt, W.D. (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.
21. Ehrbar, K., Hapfelmeier, S., Stecher, B., and Hardt, W.D. (2004) InvB is required for type III-dependent secretion of SopA in Salmonella enterica serovar Typhimurium. J Bacteriol 186: 1215-1219.
22. Elliott, S.J., Wainwright, L.A., McDaniel, T.K., Jarvis, K.G., Deng, Y.K., Lai, L.C., et al. (1998) The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28: 1-4.
23. Elliott, S.J., Hutcheson, S.W., Dubois, M.S., Mellies, J.L., Wainwright, L.A., Batchelor, M., et al. (1999) Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol Microbiol 33: 1176-1189.
24. Evdokimov, A.G., Tropea, J.E., Routzahn, K.M., and Waugh, D.S. (2002) Three-dimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr D Biol Crystallogr 58: 398-406.
25. Garmendia, J., Phillips, A.D., Carlier, M.F., Chong, Y., Schuller, S., Marches, O., et al. (2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6: 1167-1183.
26. Gauthier, A., and Finlay, B.B. (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.
27. Gauthier, A., Puente, J.L., and Finlay, B.B. (2003) Secretin of the enteropathogenic Escherichia coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun 71: 3310-3319.
28. Ghosh, P. (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
29. Goosney, D.L., DeVinney, R., Pfuetzner, R.A., Frey, E.A., Strynadka, N.C., and Finlay, B.B. (2000) Enteropathogenic E. coli translocated intimin receptor, Tir, interacts directly with alpha-actinin. Curr Biol 10: 735-738.
30. Gruenheid, S., DeVinney, R., Bladt, F., Goosney, D., Gelkop, S., Gish, G.D., et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3: 856-859.
31. Gruenheid, S., Sekirov, I., Thomas, N.A., Deng, W., O'Donnell, P., Goode, D., et al. (2004) Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 51: 1233-1249.
32. Harlow, E., and Lane, D. (1999) Using Antibodies: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
33. Hoiczyk, E., and Blobel, G. (2001) Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc Natl Acad Sci USA 98: 4669-4674.
34. Jerse, A.E., Yu, J., Tall, B.D., and Kaper, J.B. (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci USA 87: 7839-7843.
35. Kanack, K.J., Crawford, J.A., Tatsuno, I., Karmali, M., and Kaper, J.B. (2005) SepZ/EspZ is secreted and translocated into HeLa cells by the enteropathogenic Escherichia coli type III secretion system. Infect Immun 73: 4327-4337.
36. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
37. Kenny, B. (1999) Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol Microbiol 31: 1229-1241.
38. Kenny, B., and Warawa, J. (2001) Enteropathogenic Escherichia coli (EPEC) Tir receptor molecule does not undergo full modification when introduced into host cells by EPEC-independent mechanisms. Infect Immun 69: 1444-1453.
39. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A., and Finlay, B.B. (1997a) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511-520.
40. Kenny, B., Abe, A., Stein, M., and Finlay, B.B. (1997b) Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect Immun 65: 2606-2612.
41. Kenny, B., Ellis, S., Leard, A.D., Warawa, J., Mellor, H., and Jepson, M.A. (2002) Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol Microbiol 44: 1095-1107.
42. Kresse, A.U., Beltrametti, F., Muller, A., Ebel, F., and Guzman, C.A. (2000) Characterization of SepL of enterohemorrhagic Escherichia coli. J Bacteriol 182: 6490-6498.
43. Lee, S.H., and Galan, J.E. (2003) InvB is a type III secretion-associated chaperone for the Salmonella enterica effector protein SopE. J Bacteriol 185: 7279-7284.
44. Lee, S.H., and Galan, J.E. (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51: 483-495.
45. Levine, M.M., Bergquist, E.J., Nalin, D.R., Waterman, D.H., Hornick, R.B., Young, C.R., and Sotman, S. (1978) Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are noninvasive. Lancet 1: 1119-1122.
46. Lloyd, S.A., Norman, M., Rosqvist, R., and Wolf-Watz, H. (2001) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 39: 520-531.
47. Losada, L.C., and Hutcheson, S.W. (2005) Type III secretion chaperones of Pseudomonas syringae protect effectors from Lon-associated degradation. Mol Microbiol 55: 941-953.
48. Luo, Y., Frey, E.A., Pfuetzner, R.A., Creagh, A.L., Knoechel, D.G., Haynes, C.A., et al. (2000) Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 405: 1073-1077.
49. Luo, Y., Bertero, M.G., Frey, E.A., Pfuetzner, R.A., Wenk, M.R., Creagh, L., et al. (2001) Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 8: 1031-1036.
50. Marches, O., Ledger, T.N., Boury, M., Ohara, M., Tu, X., Goffaux, F., et al. (2003) Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 50: 1553-1567.
51. Matsuzawa, T., Kuwae, A., Yoshida, S., Sasakawa, C., and Abe, A. (2004) Enteropathogenic Escherichia coli activates the RhoA signaling pathway via the stimulation of GEF-H1. EMBO J 23: 3570-3582.
52. Mellies, J.L., Navarro-Garcia, F., Okeke, I., Frederickson, J., Nataro, J.P., and Kaper, J.B. (2001) espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect Immun 69: 315-324.
53. Mundy, R., Petrovska, L., Smollett, K., Simpson, N., Wilson, R.K., and Yu, J., et al. (2004) Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 72: 2288-2302.
54. Neves, B.C., Mundy, R., Petrovska, L., Dougan, G., Knutton, S., and Frankel, G. (2003) CesD2 of enteropathogenic Escherichia coli is a second chaperone for the type III secretion translocator protein EspD. Infect Immun 71: 2130-2141.
55. Nougayrede, J.P., and Donnenberg, M.S. (2004) Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol 6: 1097-1111.
56. Page, A.L., and Parsot, C. (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11.
57. Page, A.L., Sansonetti, P., and Parsot, C. (2002) Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol Microbiol 43: 1533-1542.
58. Parsot, C., Hamiaux, C., and Page, A.L. (2003) The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 6: 7-14.
59. Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
60. Phillips, N., Hayward, R.D., and Koronakis, V. (2004) Phosphorylation of the enteropathogenic E. coli receptor by the Src-family kinase c-Fyn triggers actin pedestal formation. Nat Cell Biol 6: 618-625.
61. Rosenshine, I., Ruschkowski, S., Stein, M., Reinscheid, D.J., Mills, S.D., and Finlay, B.B. (1996) A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J 15: 2613-2624.
62. Russmann, H., Kubori, T., Sauer, J., and Galan, J.E. (2002) Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol 46: 769-779.
63. Sanchez-SanMartin, C., Bustamante, V.H., Calva, E., and Puente, J.L. (2001) Transcriptional regulation of the orf19 gene and the tir-cesT-eae operon of enteropathogenic Escherichia coli. J Bacteriol 183: 2823-2833.
64. Schubot, F.D., Jackson, M.W., Penrose, K.J., Cherry, S., Tropea, J.E., Piano, G.V., and Waugh, D.S. (2005) Three-dimensional structure of a macromolecular assembly that regulates type III secretion in Yersinia pestis. J Mol Biol 346: 1147-1161.
65. Stebbins, C.E., and Galan, J.E. (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81.
66. Stebbins, C.E., and Galan, J.E. (2003) Priming virulence factors for delivery into the host. Nat Rev Mol Cell Biol 4: 738-743.
67. Thomas, J., Stafford, G.P., and Hughes, C. (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.
68. Tu, X., Nisan, I., Yona, C., Hanski, E., and Rosenshine, I. (2003) EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol Microbiol 47: 595-606.
69. Wainwright, L.A., and Kaper, J.B. (1998) EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol Microbiol 27: 1247-1260.