Interaction of enteropathogenic Escherichia coli with human intestinal mucosa: Role of effector proteins in brush border remodeling and formation of attaching and effacing lesions

Infection and Immunity

Volumn 73, Issue 2, 2005, Pages 1243-1251

  Shaw, Robert K ^a   Cleary, Jennifer ^a   Murphy, Michael S ^a   Frankel, Gad ^b   Knutton, Stuart ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EFFECTOR PROTEIN; PROTEIN; PROTEIN ESPB; PROTEIN ESPF; PROTEIN ESPG; PROTEIN ESPH; PROTEIN MAP; PROTEIN TIR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BRUSH BORDER; CONTROLLED STUDY; ESCHERICHIA COLI; HOST CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE CELL; INTESTINE MUCOSA; MICROVILLUS; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; SMALL INTESTINE; WILD TYPE;

ADHESINS, BACTERIAL; DUODENUM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON, SCANNING; MICROVILLI; RECEPTORS, CELL SURFACE;

EID: 12844281912     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.2.1243-1251.2005     Document Type: Article

References (41)

1. Bieber, D., S. W. Ramer, C. Y. Wu, W. J. Murray, T. Tobe, R. Fernandez, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
2. Campellone, K. G., and J. M. Leong. 2003. Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr. Opin. Microbiol. 6:82-90.
3. Cleary, J., L.-C. Lai, R. K. Shaw, A. Straatman-Iwanowska, M. S. Donnenberg, G. Frankel, and S. Knutton. 2004. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150:527-538.
4. Collington, G. K., I. W. Booth, and S. Knutton. 1998. Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection. Gut 42:200-207.
5. Crane, J. K., B. P. McNamara, and M. S. Donnenberg. 2001. Role of EspF in host cell death induced by enteropathogenic Escherichia coli. Cell Microbiol. 3:197-211.
6. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
7. 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.
8. 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.
9. 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.
10. Frankel, G., A. D. Phillips, L. R. Trabulsi, S. Knutton, G. Dougan, and S. Matthews. 2001. Intimin and the host cell-is it bound to end in Tir(s)? Trends Microbiol. 9:214-218.
11. Giron, J. A., A. S. Ho, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254:710-713.
12. Gruenheid, S., I. Sekirov, N. A. Thomas, W. Deng, P. O'Donnell, D. Goode, Y. Li, E. A. Frey, N. F. Brown, P. Metalnikov, T. Pawson, K. Ashman, and B. B. Finlay. 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.
13. Hartland, E. L., M. Batchelor, R. M. Delahay, C. Hale, S. Matthews, G. Dougan, S. Knutton, I. Connerton, and G. Frankel. 1999. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol. Microbiol. 32:151-158.
14. 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.
15. 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.
16. 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.
17. 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.
18. Kenny, B., S. Ellis, A. D. Leard, J. Warawa, H. Mellor, and M. A. Jepson. 2002. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol. Microbiol. 44:1095-1107.
19. Kenny, B., and M. Jepson. 2000. Targeting of an enteropathogenic E. coli (EPEC) effector protein to host mitochondria. Cell Microbiol. 2:579-590.
20. Knutton, S. 1995. Electron microscopical methods in adhesion. Methods Enzymol. 253:145-158.
21. Knutton, S., J. Adu-Bobie, C. Bain, A. D. Phillips, G. Dougan, and G. Frankel. 1997. Down regulation of intimin expression during attaching and effacing enteropathogenic Escherichia coli adhesion. Infect. Immun. 65:1644-1652.
22. Knutton, S., T. Baldwin, P. H. Williams, and A. S. McNeish. 1989. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 57:1290-1298.
23. 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.
24. 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.
25. Knutton, S., R. K. Shaw, R. P. Anantha, M. S. Donnenberg, and A. A. Zorgani. 1999. The type IV bundle-forming pilus of enteropathogenic Escherichia coli undergoes dramatic alterations in structure associated with bacterial adherence, aggregation and dispersal. Mol. Microbiol. 33:499-509.
26. Kodama, T., Y. Akeda, G. Kono, A. Takahashi, K. Imura, T. Iida, and T. Honda. 2002. The EspB protein of enterohacmorrhagic Escherichia coli interacts directly with alpha-catenin. Cell Microbiol. 4:213-222.
27. Levine, M. M., E. J. Bergquist, D. R. Nalin, D. H. Waterman, R. B. Hornick, C. R. Young, and S. Sotman. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable entcrotoxins and are non-invasive. Lancet i:1119-1122.
28. 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.
29. 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.
30. McNamara, B. P., A. Koutsouris, C. B. O'Connell, J. P. Nougayrede, M. S. Donnenberg, and G. Hecht. 2001. Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J. Clin. Investig. 107:621-629.
31. Muza-Moons, M. M., E. Schneeberger, and G. A. Hecht. 2004. Enteropathogenic Escherichia coli infection leads to appearance of aberrant tight junctions strands in the lateral membrane of intestinal epithelial cells. Cell. Microbiol. 6:783-793.
32. Rothbaum, R. J., J. C. Partin, K. Saalfield, and A. J. McAdams. 1983. An ultrastructural study of enteropathogenic Escherichia coli infection in human infants. Ultrastruct. Pathol. 4:291-304.
33. Sinclair, H. B., and A. D. O'Brien. 2002. Cell-surface localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem. 277:2876-2885.
34. Sinclair, J. F., and A. D. O'Brien. 2004. Intimin types α, β, and γ bind to nucleolin with equivalent affinity but lower avidity than to the translocated intimin receptor. J. Biol. Chem. 279:33751-33758.
35. 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.
36. Taylor, K. A., C. B. O'Connell, P. W. Luther, and M. S. Donnenberg. 1998. The EspB protein of enteropathogenic Escherichia coli is targeted to the cytoplasm of infected HeLa cells. Infect. Immun. 66:5501-5507.
37. Tu, X., I. Nisan, C. Yona, E. Hanski, and I. Rosenshine. 2003. EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol. Microbiol. 47:595-606.
38. Wilson, R., R. K. Shaw, S. Daniell, I. Rosenshine, S. Aizawa, 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.
39. 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.
40. Yoshida, S., E. Katayama, A. Kuwae, H. Mimuro, T. Suzuki, and C. Sasakawa. 2002. Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J. 21:2923-2935.
41. Zhang, H. Z., and M. S. Donnenberg. 1996. DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol. Microbiol. 21:787-797.