Invasion of epithelial cells by locus of enterocyte effacement-negative enterohemorrhagic Escherichia coli

Infection and Immunity

Volumn 73, Issue 5, 2005, Pages 3063-3071

  Luck, Shelley N ^a   Bennett Wood, Vicki ^b,c   Poon, Rachael ^a   Robins Browne, Roy M ^b,c   Hartland, Elizabeth L ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COLCHICINE; COMPACTIN; CYTOCHALASIN D; ENZYME INHIBITOR; GENISTEIN; GENTAMICIN; PROTEIN TYROSINE KINASE INHIBITOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL INVASION; CELL LINE; CELL MEMBRANE; CELL STRAIN CACO 2; CELL SURFACE; CELL TRANSPORT; CELL VACUOLE; CHO CELL; CONTROLLED STUDY; ENTEROBACTER; EPITHELIUM CELL; ESCHERICHIA COLI O157; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL ADHESION; CACO-2 CELLS; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; ENTEROCYTES; ESCHERICHIA COLI; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PHOSPHOPROTEINS;

EID: 17644427391     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.5.3063-3071.2005     Document Type: Article

References (57)

1. Adam, T., M. Giry, P. Boquet, and P. Sansonetti. 1996. Rho-dependent membrane folding causes Shigella entry into epithelial cells. EMBO J. 15:3315-3321.
2. Alrutz, M. A., and R. R. Isberg. 1998. Involvement of focal adhesion kinase in invasin-mediated uptake. Proc. Natl. Acad. Sci. USA 95:13658-13663.
3. Alrutz, M. A., A. Srivastava, K. W. Wong, C. D'Souza-Schorey, M. Tang, L. E. Ch'Ng, S. B. Snapper, and R. R. Isberg. 2001. Efficient uptake of Yersinia pseudotuberculosis via integrin receptors involves a Rac1-Arp 2/3 pathway that bypasses N-WASP function. Mol. Microbiol. 42:689-703.
4. Bennett-Wood, V. R., J. Russell, A. M. Bordun, P. D. Johnson, and R. M. Robins-Browne. 2004. Detection of enterohaemorrhagic Escherichia coli in patients attending hospital in Melbourne, Australia. Pathology 36:345-351.
5. Biswas, D., K. Itoh, and C. Sasakawa. 2000. Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol. Med. Microbiol. 29:203-211.
6. Bonnet, R., B. Souweine, G. Gauthier, C. Rich, V. Livrelli, J. Sirot, B. Joly, and C. Forestier. 1998. Non-O157:H7 Stx2-producing Escherichia coli strains associated with sporadic cases of hemolytic-uremic syndrome in adults. J. Clin. Microbiol. 36:1777-1780.
7. Boudeau, J., N. Barnich, and A. Darfeuille-Michaud. 2001. Type 1 pili-mediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol. Microbiol. 39:1272-1284.
8. Boudeau, J., A. L. Glasser, E. Masseret, B. Joly, and A. Darfeuille-Michaud. 1999. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect. Immun. 67:4499-4509.
9. Chen, L. M., S. Hobbie, and J. E. Galan. 1996. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274:2115-2118.
10. Clausen, J. D., G. Christiansen, H. U. Holst, and S. Birkelund. 1997. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol. Microbiol. 25:441-449.
11. Cowan, C., H. A. Jones, Y. H. Kaya, R. D. Perry, and S. C. Straley. 2000. Invasion of epithelial cells by Yersinia pestis: evidence for a Y. pestis-specific invasin. Infect. Immun. 68:4523-4530.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
13. Dean-Nystrom, E. A., A. R. Melton-Celsa, J. F. Pohlenz, H. W. Moon, and A. D. O'Brien. 2003. Comparative pathogenicity of Escherichia coli O157 and intimin-negative non-O157 Shiga toxin-producing E coli strains in neonatal pigs. Infect. Immun 71:6526-6533.
14. Doughty, S., J. Sloan, V. Bennett-Wood, M. Robertson, R. M. Robins-Browne, and E. L. Hartland. 2002. Identification of a novel fimbrial gene cluster related to long polar fimbriae in locus of enterocyte effacement-negative strains of enterohemorrhagic Escherichia coli. Infect. Immun. 70:6761-6769.
15. Dytoc, M. T., A. Ismaili, D. J. Philpott, R. Soni, J. L. Brunton, and P. M. Sherman. 1994. Distinct binding properties of eaeA-negative verocytotoxin-producing Escherichia coli of serotype O113:H21. Infect. Immun. 62:3494-3505.
16. Elliott, E. J., R. M. Robins-Browne, E. V. O'Loughlin, V. Bennett-Wood, J. Bourke, P. Henning, G. G. Hogg, J. Knight, H. Powell, and D. Redmond. 2001. Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features. Arch. Dis. Child. 85:125-131.
17. Elsinghorst, E. A., L. S. Baron, and D. J. Kopecko. 1989. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli. Proc. Natl. Acad. Sci. USA 86:5173-5177.
18. Finlay, B. B., and S. Falkow. 1988. Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie 70:1089-1099.
19. Francis, C. L., A. E. Jerse, J. B. Kaper, and S. Falkow. 1991. Characterization of interactions of enteropathogenic Escherichia coli O127:H6 with mammalian cells in vitro. J Infect. Dis. 164:693-703.
20. 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.
21. Gruenheid, S., and B. B. Finlay. 2003. Microbial pathogenesis and cytoskeletal function. Nature 422:775-781.
22. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
23. Hogan, M. C., J. M. Gloor, J. R. Uhl, F. R. Cockerill, and D. S. Milliner. 2001. Two cases of non-O157:H7 Escherichia coli hemolytic uremic syndrome caused by urinary tract infection. Am. J. Kidney Dis. 38:E22.
24. Hu, L., and D. J. Kopecko. 1999. Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun. 67:4171-4182.
25. Isberg, R. R., Z. Hamburger, and P. Dersch. 2000. Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect. 2:793-801.
26. Jepson, M. A., S. Pellegrin, L. Peto, D. N. Banbury, A. D. Leard, H. Mellor, and B. Kenny. 2003. Synergistic roles for the Map and Tir effector molecules in mediating uptake of enteropathogenic Escherichia coli (EPEC) into non-phagocytic cells. Cell Microbiol. 5:773-783.
27. Karmali, M. A., M. Petric, C. Lim, P. C. Fleming, G. S. Arbus, and H. Lior. 1985. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151:775-782.
28. 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.
29. Levine, M. M., J. P. Nataro, H. Karch, M. M. Baldini, J. B. Kaper, R. E. Black, M. L. Clements, and A. D. O'Brien. 1985. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
30. Leyton, D. L., J. Sloan, R. E. Hill, S. Doughty, and E. L. Hartland. 2003. Transfer region of pO113 from enterohemorrhagic Escherichia coli: similarity with R64 and identification of a novel plasmid-encoded autotransporter, EpeA. Infect. Immun. 71:6307-6319.
31. Lindgren, S. W., A. R. Melton, and A. D. O'Brien. 1993. Virulence of enterohemorrhagic Escherichia coli O91:H21 clinical isolates in an orally infected mouse model. Infect. Immun 61:3832-3842.
32. Marches, O., J. P. Nougayrede, S. Boullier, J. Mainil, G. Charlier, I. Raymond, P. Pohl, M. Boury, J. De Rycke, A. Milon, and E. Oswald. 2000. Role of tir and intimin in the virulence of rabbit enteropathogenic Escherichia coli serotype O103:H2. Infect. Immun. 68:2171-2182.
33. Martinez, J. J., and S. J. Hultgren. 2002. Requirement of Rho-family GT-Pases in the invasion of type 1-piliated uropathogenic Escherichia coli. Cell Microbiol. 4:19-28.
34. Martinez, J. J., M. A. Mulvey, J. D. Schilling, J. S. Pinkner, and S. J. Hultgren. 2000. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 19:2803-2812.
35. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
36. 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.
37. McKee, M. L., A. R. Melton-Celsa, R. A. Moxley, D. H. Francis, and A. D. O'Brien. 1995. Enterohemorrhagic Escherichia coli O157:H7 requires intimin to colonize the gnotobiotic pig intestine and to adhere to HEp-2 cells. Infect. Immun 63:3739-3744.
38. Mounier, J., V. Laurent, A. Hall, P. Fort, M. F. Carlier, P. J. Sansonetti, and C. Egile. 1999. Rho family GTPases control entry of Shigella flexneri into epithelial cells but not intracellular motility. J. Cell Sci. 112:2069-2080.
39. Mulder, B., T. Michiels, M. Simonet, M. P. Sory, and G. Cornelis. 1989. Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect. Immun. 57:2534-2541.
40. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
41. Oelschlaeger, T. A., T. J. Barrett, and D. J. Kopecko. 1994. Some structures and processes of human epithelial cells involved in uptake of enterohemorrhagic Escherichia coli O157:H7 strains. Infect. Immun. 62:5142-5150.
42. Paton, A. W., P. Srimanote, M. C. Woodrow, and J. C. Paton. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009.
43. Paton, A. W., M. C. Woodrow, R. M. Doyle, J. A. Lanser, and J. C. Paton. 1999. Molecular characterization of a Shiga toxigenic Escherichia coli O113: H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J. Clin. Microbiol. 37:3357-3361.
44. Paton, J. C., and A. W. Paton. 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
45. Perna, N. T., G. Plunkett III, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfai, J. Hackett, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, and F. R. Blattner. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529-533.
46. Robins-Browne, R. M., and V. Bennett-Wood. 1992. Quantitative assessment of the ability of Escherichia coli to invade cultured animal cells. Microb. Pathog. 12:159-164.
47. Rosenshine, I., V. Duronio, and B. B. Finlay. 1992. Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect. Immun. 60:2211-2217.
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. Scott, M. E., A. R. Melton-Celsa, and A. D. O'Brien. 2003. Mutations in hns reduce the adherence of Shiga toxin-producing E. coli 091:H21 strain B2F1 to human colonic epithelial cells and increase the production of hemolysin. Microb. Pathog. 34:155-159.
50. Steele-Mortimer, O., S. Meresse, J. P. Gorvel, B. H. Toh, and B. B. Finlay. 1999. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol. 1:33-49.
51. Tacket, C. O., M. B. Sztein, G. Losonsky, A. Abe, B. B. Finlay, B. P. McNamara, G. T. Fantry, S. P. James, J. P. Nataro, M. M. Levine, and M. S. Donnenberg. 2000. Role of EspB in experimental human enteropathogenic Escherichia coli infection. Infect. Immun. 68:3689-3695.
52. Tafazoli, F., K. E. Magnusson, and L. Zheng. 2003. Disruption of epithelial barrier integrity by Salmonella enterica serovar Typhimurium requires geranylgeranylated proteins. Infect. Immun. 71:872-881.
53. Tran Van Nhieu, G., and R. R. Isberg. 1993. Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J. 12:1887-1895.
54. Tzipori, S., H. Karch, K. I. Wachsmuth, R. M. Robins-Browne, A. D. O'Brien, H. Lior, M. L. Cohen, J. Smithers, and M. M. Levine. 1987. Role of a 60-megadalton plasmid and Shiga-like toxins in the pathogenesis of infection caused by enterohemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect. Immun. 55:3117-3125.
55. Watarai, M., Y. Kamata, S. Kozaki, and C. Sasakawa. 1997. Rho, a small GTP-binding protein, is essential for Shigella invasion of epithelial cells. J. Exp. Med. 185:281-292.
56. 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.
57. Young, V. B., S. Falkow, and G. K. Schoolnik. 1992. The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J. Cell Biol. 116:197-207.