CesD2 of enteropathogenic Escherichia coli is a second chaperone for the type III secretion translocator protein EspD

Infection and Immunity

Volumn 71, Issue 4, 2003, Pages 2130-2141

  Neves, Bianca C ^a   Mundy, Rosanna ^a   Petrovska, Liljana ^a   Dougan, Gordon ^a   Knutton, Stuart ^b   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CHAPERONE; INTIMIN; PROTEIN CESD2; PROTEIN ESPD; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BINDING KINETICS; CONTROLLED STUDY; CYTOSOL; ESCHERICHIA COLI; EXTRACELLULAR SPACE; GENETIC CODE; IN VITRO STUDY; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN TRANSPORT; TRANSPORT KINETICS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CITROBACTER FREUNDII; COLON; ENTEROBACTERIACEAE INFECTIONS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C3H; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHOSPHOPROTEINS; SEQUENCE ANALYSIS, DNA; VIRULENCE;

EID: 0037379441     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.4.2130-2141.2003     Document Type: Article

References (61)

1. Abe, A., M. de Grado, R. A. Pfuetzner, C. Sanchez-Sanmartin, 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. Adu-Bobie, J., G. Frankel, C. Bain, A. G. Goncaleves, L. R. Trabulsi, G. Douce, S. Knutton, and G. Dougan. 1998. Detection of intimin α, β, γ, and δ, four intimin derivatives expressed by attaching and effacing microbial pathogens. J. Clin. Microbiol. 36:662-668.
3. Batchelor, M., S. Knutton, V. Huter, M. Zanial, G. Dougan, and G. Frankel. 1999. Development of a universal intimin antiserum and PCR primers. J. Clin. Microbiol. 37:3822-3827.
4. Bennett, J. C., and C. Hughes. 2000. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8:202-204.
5. 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.
6. Creasey, E. A., R. M. Delahay, A. A. Bishop, R. K. Shaw, B. Kenny, S. Knutton, and G. Frankel. 2002. CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol. Microbiol. 47:209-221.
7. Daniell, S. J., R. M. Delahay, R. K. Shaw, E. L. Hartland, M. J. Pallen, F. Booy, F. Ebel, S. Knutton, and G. Frankel. 2001. The coiled coil domain of enteropathogenic Escherichia coli type III secreted protein EspD is involved in EspA filament-mediated cell attachment and hemolysis. Infect. Immun. 69:4055-4064.
8. 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.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
10. Day, J. B., and G. V. Plano. 1998. A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersiniapestis. Mol. Microbiol. 30:777-788.
11. Deng. W., Y. Li, B. A. Vallance, and B. B. Finlay. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69:6323-6335.
12. Donnenberg, M. S., J. Yu, and J. B. Kaper. 1993. A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells. J. Bacteriol. 175:4670-4680.
13. Elliott, S. J., M. S. Dubois, S. W. Hutcheson, L. A. Wainwright, M. Batchelor, G. Frankel, S. 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.
14. Elliott, S. J., E. O. Krejany, J. L. Mellies, R. M. Robins-Browne, C. Sasakawa, and J. B. Kaper. 2001. EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect. Immun. 69:4027-4033.
15. Elliott, S. J., C. B. O'Connell, A. Koutsouris, C. Brinkley, M. S. Donnenberg, G. Hecht, and J. B. Kaper. 2002. A gene from the locus of enterocyte effacement that is required for entero pathogenic Escherichia coli to increase tight-junction permeability encodes a chaperone for EspF. Infect. Immun. 70:2271-2277.
16. Elliott, S. J., L. A. Wainwright, T. K. McDaniel, K. G. Jarvis, Y. K. Deng, L. C. Lai, B. P. McNamara, M. S. Donnenberg, and J. B. Kaper. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol 28:1-4.
17. 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.
18. Frankel, G., A. D. Phillips, M. Novakova, H. Field, D. C. Candy, D. B. Schauer, G. Douce, and G. Dougan. 1996. Intimin from enteropathogenic Escherichia coli restores murine virulence to a Citrobacter rodentium eaeA mutant: induction of an immunoglobulin A response to intimin and EspB. Infect. Immun. 64:5315-5325.
19. Frankel, G., A. D. Phillips, I. Rosenshine, G. Dougan, J. B. Kaper, and S. Knutton. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
20. 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 dispensable for targeting to the secretion loci. Mol. Microbiol. 16:635-647.
21. Galan, 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.
22. Ghaem-Maghami, M., C. P. Simmons, S. Daniell, M. Pizza, D. Lewis, G. Frankel, and G. Dougan. 2001. Intimin-specific immune responses prevent bacterial colonization by the attaching-effacing pathogen Citrobacter rodentium. Infect. Immun. 69:5597-5605.
23. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
24. Ilan, O., Y. Bloch, G. Frankel, H. Ullrich, K. Geider, and I. Rosenshine. 1999. Protein tyrosine kinases in bacterial pathogens are associated with virulence and production of exopolysaccharide. EMBO J. 18:3241-3248.
25. Jarvis, K. G., J. A. Giron, 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.
26. Jerse, A. E., J. Yu, B. D. Tall, and J. B. Kaper. 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.
27. Kellermann, O., and S., Szmelcman. 1974. Active transport of maltose in Escherichia coli K12. Involvement of a "periplasmic" maltose binding protein. Eur. J. Biochem. 47:139-149.
28. Kenny, B., R. DeVinney, M. Stein, D. J. Reinscheid, E. A. Frey, and B. B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-520.
29. Kenny, B., and M. Jepson. 2000. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell. Microbiol. 2:579-590.
30. Kenny, B., L. C. Lai, B. B. Finlay, and M. S. Donnenberg. 1996. EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells. Mol. Microbiol. 20:313-323.
31. Knutton, S., D. R. Lloyd, and A. S. McNeish. 1987. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect. Immun. 55:69-77.
32. 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.
33. Kubori, T., Y. Matsushima, D. Nakamura, J. Uralil, M. Lara-Tejero, A. Sukhan, J. E. Galan, and S. I. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602-605.
34. Lai, L. C., L. A. Wainwright, K. D. Stone, and M. S. Donnenberg. 1997. A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells. Infect. Immun. 65:2211-2217.
35. Lee, C., P. Li, H. Inouye, E. R. Brickman, and J. Beckwith. 1989. Genetic studies on the inability of β-galactosidase to be translocated across the Escherichia coli cytoplasmic membrane. J. Bacteriol. 171:4609-4616.
36. Levine, M. M., E. J. Berquist, D. R. Nalin, D. H. Waterman, R. B. Hornick, C. R. Young, S. Stoman, and B. Rowe. 1978. Escherichia coli that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet i:119-122.
37. 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.
38. McNamara, B. P., and M. S. Donnenberg. 1998. A novel proline-rich protein, EspF, is secreted from enteropathogenic Escherichia coli via the type III export pathway. FEMS Microbiol. Lett. 166:71-78.
39. McNamara, B. P., A. Koutsouris, C. B. O'Connell, J. P. Nougayrede, M. S. Donnenberg, and G. Hecht. 2000. Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J. Clin. Investig. 107:621-629.
40. Mellies, J. L., S. J. Elliott, V. Sperandio, M. S. Donnenberg, and J. B. Kaper. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33:296-306.
41. Moon, H. W., S. C. Whipp, R. A. Argenzio, M. M. Levine, and R. A. Giannella. 1983. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41:1340-1351.
42. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
43. Newman, J. V., B. A. Zabel, S. S. Jha, and D. B. Schauer. 1999. Citrobacter rodentium espB is necessary for signal transduction and for infection of laboratory mice. Infect. Immun. 67:6019-6025.
44. 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.
45. Robins-Browne, R. M., A. M. Tokhi, L. M. Adams, V. Bennett-Wood, A. V. Moisidis, E. O. Krejany, and L. E. O'Gorman. 1994. Adherence characteristics of attaching and effacing strains of Escherichia coli from rabbits. Infect. Immun. 62:1584-1592.
46. Rosenshine, I., S. Ruschkowski, M. Stein, D. J. Reinscheid, S. D. Mills, and B. B. Finlay. 1996. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J. 15:2613-2624.
47. Schauer, D. B., and S. Falkow. 1993. Attaching and effacing locus of a Citrobacter freundii biotype 4280 that causes transmissible murine colonic hyperplasia. Infect. Immun. 61:2486-2492.
48. Schauer, D. B., and S. Falkow. 1993. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect. Immun. 61:4654-4661.
49. 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.
50. Simmons, C. P., N. S. Goncalves, M. Ghaem-Maghami, M. Bajaj-Elliott, S. Clare, B. Neves, G. Frankel, G. Dougan, and T. T. MacDonald. 2002. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen. Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J. Immunol. 15:1804-1812.
51. 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. 19 EMBO J. 3876-3887.
52. Taylor, K. A., P. W. Luther, and M. S. Donnenberg. 1999. Expression of the EspB protein of enteropathogenic Escherichia coli within HeLa cells affects stress fibers and cellular morphology. Infect. Immun. 67:120-125.
53. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
54. Tzipori, S., I. K. Wachsmuth, C. Chapman, R. Birden, J. Brittingham, C. Jackson, and J. Hogg. 1986. The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157:H7 in gnotobiotic piglets. J. Infect. Dis. 154:712-714.
55. Wachter, C., C. Beinke, M. Mattes, and M. A. Schmidt. 1999. Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 31:1695-1707.
56. Wainwright, L. A., and J. B. Kaper. 1998. EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol. Microbiol. 27:1247-1260.
57. 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.
58. Wattiau, P., S. Woestyn, and G. R. Cornelis. 1996. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20:255-262.
59. 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.
60. 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.
61. Wolff, C., I. Nisan, E. Hanski, G. Frankel, and I. Rosenshine, 1998. Protein translocation into HeLa cells by infecting enteropathogenic Escherichia coli. Mol. Microbiol. 28:143-155.