Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis

Microbiology

Volumn 150, Issue 11, 2004, Pages 3631-3645

  Dziva, Francis ^a   van Diemen, Pauline M ^a   Stevens, Mark P ^a   Smith, Amanda J ^a   Wallis, Timothy S ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; BACTERIUM MUTANT; CATTLE; CONTROLLED STUDY; ESCHERICHIA COLI O157; FIMBRIA; GASTROINTESTINAL TRACT; GENE DELETION; GENE IDENTIFICATION; GENE INSERTION; GENE SEQUENCE; INTESTINE CELL; INTESTINE EPITHELIUM; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; TRANSPOSON;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CATTLE; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; FECES; FIMBRIAE, BACTERIAL; GASTROINTESTINAL TRACT; GENES, BACTERIAL; MUTAGENESIS, INSERTIONAL; PHOSPHOPROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VIRULENCE FACTORS;

BOVINAE; ESCHERICHIA COLI; SHIGELLA;

EID: 9144262494     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27448-0     Document Type: Article

References (92)

1. Ammon, A. (1997). Surveillance of enterohaemorrhagic Escherichia coli (EHEC) infections and haemolytic uraemic syndrome (HUS) in Europe. Euro Surveill 2, 91-96.
2. Batisson, I., Guimond, M. P., Girard, F., An, H., Zhu, C., Oswald, E., Fairbrother, J. M., Jacques, M. & Harel, J. (2003). Characterization of the novel factor paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli. Infect Immun 71, 4516-4525.
3. Bettelheim, K. A. (2000). The role of non-O157 VTEC. Symp Ser Soc Appl Microbiol 29, 38S-50S.
4. Bilge, S. S., Vary, J. C. S., Jr, Dowell, S. F. & Tarr, P. I. (1996). Role of the Escherichia coli O157:H7 O side chain in adherence and analysis of an rfb locus. Infect Immun 64, 4795-4801.
5. Borczyk A. A., Karmali, M. A., Lior, H. & Duncan, L. M. C. (1987). Bovine reservoir for verotoxin-producing Escherichia coli O157:H7. Lancet 10, 98.
6. Brown, C. A., Harmon, B. G., Zhao, T. & Doyle, M. P. (1997). Experimental Escherichia coli O157:H7 carriage in calves. Appl Environ Microbiol 63, 27-32.
7. Buchrieser, C., Glaser, P., Rusniok, C., Nedjari, H., D'Hauteville, H., Kunst, F., Sansonetti, P. & Parsot, C. (2000). The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38, 760-771.
8. Cleary, J., Lai, L. C., Shaw, R. K., Straatman-Iwanowska, A., Donnenberg, M. S., Frankel, G. & Knutton, S. (2004). Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150, 527-538.
9. Cockerill, F., 3rd, Beebakhee, G., Soni, R. & Sherman, P. (1996). Polysaccharide side chains are not required for attaching and effacing adhesion of Escherichia coli O157:H7. Infect Immun 64, 3196-3200.
10. Cornick, N. A., Booher, S. L. & Moon, H. W. (2002). Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect Immun 70, 2704-2707.
11. Cray, W. C., Jr & Moon, H. W. (1995). Experimental infection of calves and adult cattle with Escherichia coli O157:H7. Appl Environ Microbiol 61, 1586-1590.
12. Datsenko, K. A. & Wanner, B. L. (2000). One step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
13. Dean-Nystrom, E. A., Bosworth, B. T., Cray, W. C., Jr & Moon, H. W. (1997). Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun 65, 1842-1848.
14. Dean-Nystrom, E. A., Bosworth, B. T., Moon, H. W. & O'Brien, A. D. (1998). Escherichia coli O157:H7 requires intimin for enteropathogenicity. Infect Immun 66, 4560-4563.
15. Dean-Nystrom, E. A., Bosworth, B. T. & Moon, H. W. (1999). Pathogenesis of Escherichia coli O157:H7 in weaned calves. Adv EXP Med Biol 473, 173-177.
16. Deng, W., Puente, J. L., Gruenheid, S. & 15 other authors (2004). Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 101, 3597-3602.
17. DeVinney, R., Stein, M., Reinscheid, D., Abe, A., Ruschkowski, S. & Finlay, B. B. (1999). Enterohemorrhagic Escherichia coli O157:H7 produces Tir, which is translocated to the host cell membrane but is not tyrosine phosphorylated. Infect Immun 67, 2389-2398.
18. Donnenberg, M. S., Tzipori, S., McKee, M. L., O'Brien, A. D., Alroy, J. & Kaper, J. B. (1993). The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest 92, 1418-1424.
19. Dytoc, M., Soni, R., Cockerill, F., 3rd, De Azavedo, J., Louie, M., Brunton, J. & Sherman, P. (1993). Multiple determinants of verotoyin-producing Escherichia coli O157:H7 attachment-effacement. Infect Immun 61, 3382-3391.
20. Ebel, F., Podzadel, T., Rohde, M., Kresse, A. U., Kramer, S., Delbel, C., Guzman, C. A. & Chakraborty, T. (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.
21. Elder, R. O., Keen, J. E., Siragusa, G. R., Barkocy-Gallagher, G. A., Koohmaraie, M. & Laegreid, W. (2000). Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc Natl Acad Sci U S A 97, 2999-3003.
22. Elliott, S. J., O'Connell, C. B., Koutsouris, A., Brinkley, C., Donnenberg, M. S., Hecht G. & Kaper, J. B. (2002). A gene from the locus of enterocyte effacement that is required for enteropathogenic Escherichia coli to increase tight-junction permeability encodes a chaperone for EspF. Infect Immun 70, 2271-2277.
23. Fernandez-Prada, C. M., Hoover, D. L., Tall, B. D., Hartman, A. B., Kopelowitz, J. & Venkatesan, M. M. (2000). Shigella flexneri IpaH(7-8) facilitates escape of virulent bacteria from the endocytic vacuoles of mouse and human macrophages. Infect Immun 68, 3608-3619.
24. Frankel, G., Lider, O., Hershkoviz, R., Mould, A. P., Kachalsky, S. G., Candy, D. C. A., Cahalon, L., Humphries, M. J. & Dougan, G. (1996). The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J Biol Chem 271, 20359-20364.
25. Frankel, G., Phillips, A. D., Rosenshine, I., Dougan, G., Kaper, J. B. & Knutton, S. (1998). Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30, 911-921.
26. Girón, J. A., Torres, A. G., Freer, E. & Kaper, J. B. (2002). The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44, 361-379.
27. Grass, S. & St Geme, J. W., 3rd (2000). Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin: roles of the N-terminal and C-terminal domains. Mol Microbiol 36, 55-67.
28. Grauke, L. J., Kudva, I. T., Yoon, J. W., Hunt, C. W., Williams, C. J. & Hovde, C. J. (2002). Gastrointestinal tract location of Escherichia coli O157:H7 in ruminants. Appl Environ Microbiol 68, 2269-2277.
29. Hayashi, T., Makino, K., Ohnishi, M. & 19 other authors (2001). Complete genome sequence of enterohaemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8, 11-22.
30. Hensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E. & Holden, D. W. (1995). Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400-403.
31. Hoey, D. E., Currie, C., Else, R. W., Nutikka, A., Lingwood, C. A., Gaily, D. L. & Smith, D. G. (2002). Expression of receptors for verotoxin 1 from Escherichia coli O157 on bovine intestinal epithelium. J Med Microbiol 51, 143-149.
32. Ide, T., Laarmann, S., Greune, L., Schillers, H., Oberleithner, H. & Schmidt M. A. (2001). Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 3, 669-679.
33. Jepson, M. A., Pellegrin, S., Peto, L., Banbury, D. N., Leard, A. D., Mellor, H. & Kenny, B. (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.
34. Jordan, D., McEwen, S. A., Lammerding, A. M., McNab, W. B. & Wilson, J. B. (1999). Pre-slaughter control of Escherichia coli O157 in beef cattle: a simulation study. Prev Vet Med 41, 55-74.
35. Judge, N. A., Mason, H. S. & O'Brien, A. D. (2004). Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect Immun 72, 168-175.
36. Kanamaru, K., Kanamaru, K., Tatsuno, I., Tobe, T. & Sasakawa, C. (2000). SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 38, 805-816.
37. Karch, H. & Bielaszewska, M. (2001). Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157:H(-) strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis. J Clin Microbiol 39, 2043-2049.
38. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C. & Steele, B. T. (1983). Escherichia coli cytotoxin, haemolytic-uraemic syndrome, and haemorrhagic colitis. Lancet ii, 1299-1300.
39. Kenny, B. & Jepson, M. (2000). Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2, 579-590.
40. Kenny, B., Ellis, S., Leard, A. D., Warawa, J., Mellor, H. & 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.
41. Klapproth, J. M., Scaletsky, I. C., McNamara, B. P., Lai, L. C., Malstrom, C., James, S. P. & Donnenberg, M. S. (2000). A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect Immun 68, 2148-2155.
42. Koo, J. T., Choe, J. & Moseley, S. L. (2004). HrpA, a DEAH-box RNA helicase, is involved in mRNA processing of a fimbrial operon in Escherichia coli. Mol Microbiol 52, 1813-1826.
43. Kresse, A. U., Rohde, M. & Guzman, C. A. (1999). The EspD protein of enterohemorrhagic Escherichia coli is required for the formation of bacterial surface appendages and is incorporated in the cytosplasmic membranes of target cells. Infect Immun 67, 4834-4842.
44. Liebler, E. M., Pohlenz, J. F. & Woode, G. N. (1988). Gut-associated lymphoid tissue in the large intestine of calves. I. Distribution and histology. Vet Pathol 25, 503-508.
45. Locking, M. E. O'Brien S. J., Reilly, W. J., Wright, E. M., Campbell, D. M., Coia, J. E., Browning, L. M. & Ramsay, C. N. (2001). Risk factors for sporadic cases of Escherichia coli O157 infection: the importance of contact with animal excreta. Epidemiol Infect 127, 215-220.
46. Martindale, J., Stroud, D., Moxon, E. R. & Tang, C. M. (2000). Genetic analysis of Escherichia coli K1 gastrointestinal colonisation. Mol Microbiol 37, 1293-1305.
47. McKee, M. L., Melton-Celsa, A. R., Moxley, R. A., Francis, D. H. & O'Brien, A. D. (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.
48. McNally, A., Roe, A. J., Simpson, S., Thomson-Carter, F. M., Hoey, D. E., Currie, C., Chakraborty, T., Smith, D. G. & Gally, D. L. (2001). Differences in levels of secreted locus of enterocyte effacement proteins between human disease-associated and bovine Escherichia coli O157. Infect Immun 69, 5107-5114.
49. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. & Tauxe, R. V. (1999). Food-related illness and death in the United States. Emerg Infect Dis 5, 607-625.
50. Menge, C., Stamm, I., van Diemen, P. M., Sopp, P., Baljer, G., Wallis, T. S. & Stevens, M. P. (2004). Phenotypic and functional characterization of intraepithelial lymphocytes in a bovine ligated intestinal loop model of enterohaemorrhagic Escherichia coli infection. J Med Microbiol 53, 573-579.
51. Michino, H., Araki, K., Minami, S., Takaya, S., Sakai, N., Miyazaki, M., Ono, A. & Yanagawa, H. (1999). Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan associated with consumption of white radish sprouts. Am J Epidemiol 150, 787-796.
52. Mundy, R., Pickard, D., Wilson, R. K., Simmons, C. P., Dougan, G. & Frankel, G. (2003). Identification of a novel pilus gene cluster required for gastrointestinal colonisation of Citrobacter rodentium. Mol Microbiol 48, 795-809.
53. Mundy, R., Petrovska, L., Smollett, K. & 8 other authors (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. Nagano, K., Taguchi, K., Hara, T., Yokoyama, S., Kawada, K. & Mori, H. (2003). Adhesion and colonization of enterohemorrhagic Escherichia coli O157:H7 in cecum of mice. Microbiol Immunol 47, 125-132.
55. Nataro, J. P. & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142-201.
56. Naylor, S. W., Low, J. C., Besser, T. E., Mahajan, A., Gunn, G. J., Pearce, M. C., McKendrick, I. J., Smith, D. G. & Gaily, D. L. (2003). Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71, 1505-1512.
57. Nicholls, L., Grant T. H. & Robins-Browne, R. M. (2000). Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelia] cells. Mol Microbiol 35, 275-288.
58. O'Brien, S. J., Adak, G. K. & Gilham, C. (2001). Contact with farming environment as a major risk factor for Shiga toxin (Verocytotoxin)-producing Escherichia coli O157 infection in humans. Emerg Infect Dis 7, 1049-1051.
59. Orskov, F., Orskov, I. & Villar, J. A. (1987). Cattle as a reservoir of verotoyin-producing Escherichia coli O157:H7. Lancet 10, 276.
60. Paiba, G. A., Gibbens, J. C., Pascoe, S. J. & 12 other authors (2002). Faecal carriage of verocytotoxin-producing Escherichia coli O157 in cattle and sheep at slaughter in Great Britain. Vet Rec 150, 593-598.
61. Parsons, K. R., Bland, A. P. & Hall, G. A. (1991). Follicle associated epithelium of the gut associated lymphoid tissue of cattle. Vet Pathol 28, 22-29.
62. Paton, J. C. & Paton, A. W. (1998). Pathogenesis and diagnosis of Shiga-toxin producing Escherichia coli infections. Clin Microbiol Rev 11, 450-479.
63. Paton, A. W., Voss, E., Manning, P. A. & Paton, J. C. (1998). Antibodies to lipopolysaccharide block adherence of Shiga toxin-producing Escherichia coli to human intestinal epithelial (Henle407) cells. Microb Pathol 24, 57-63.
64. Paton, A. W., Srimanote, P., Woodrow, M. C. & Paton, J. C. (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.
65. Perna, N. T., Plunket, G., 3rd, Burland, V. & 25 other authors (2001). Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409, 529-533.
66. Potter, A. A., Klashinsky, S., Li, Y. & 9 other authors (2004). Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 22, 362-369.
67. Riley, L. W., Remis, R. S., Helgerson, S. D. & 9 other authors (1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308, 681-685.
68. Ritchie, J. M., Thorpe, C. M., Rogers, A. B. & Waldor, M. K. (2003). Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 71, 7129-7139.
69. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edition. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
70. Sherman, P. & Soni, R. (1988). Adherence of Vero cytotoxin-producing Escherichia coli of serotype O157:H7 to human epithelial cells in tissue culture: the role of outer membranes as bacterial adhesins. J Med Microbiol 26, 11-17.
71. Sherman, P., Cockerill, F., 3rd, Soni, R. & Brunton, J. (11991). Outer membranes are competitive inhibitors of Escherichia coli O157:H7 adherence to epithelial cells. Infect Immun 59, 890-899.
72. Simon, R., Preifer, U. & Puhler, A. (1983). A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1, 784-791.
73. Sinclair, J. F. & O'Brien, A. D. (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.
74. St Geme, J. W., 3rd, Falkow, S. & Barenkamp, S. J. (1993). High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci U S A 90, 2875-2879.
75. Stevens, M. P., van Diemen, P. M., Dziva, F., Jones, P. W. & Wallis, T. S. (2002a). Options for the control of enterohaemorrhagic Escherichia coli in ruminants. Microbiology 148, 3767-3778.
76. Stevens, M. P., van Diemen, P. M., Frankel, G., Phillips, A. D. & Wallis, T. S. (2002b). Efa1 influences colonization of the bovine intestine by Shiga toxin-producing Escherichia coli serotypes; O5 and O111. Infect Immun 70, 5158-5166.
77. Stevens, M. P., Roe, A. J., Vlisidou, I., van Diemen, P. M., La Ragione, R. M., Best, A., Woodward, M. J., Gally, D. L. & Wallis, T. S. (2004). Mutation of toxB and a truncated version of the efa1 gene in Escherichia coli O157:H7 influences the expression and secretion of locus of enterocyte effacement-encoded proteins but not intestinal colonization in calves or sheep. Infect Immun 72, 5402-5411.
78. Tarr, P. I., Bilge, S. S., Vary, J. C., Jr, Jelcic, S., Habeeb, R. L., Ward, T. R., Baylor, M. R. & Besser, T. E. (2000 . Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68, 1400-1407.
79. Tatsuno, I., Kimura, H., Okutani, A. & 10 other authors (2000). Isolation and characterization of mini-Tn5Km2 insertion mutants of enterohemorrhagic Escherichia coli O157:H7 deficient in adherence to Caco-2 cells. Infect Immun 68, 5943-5952.
80. Tatsuno, I., Horie, M., Abe, H. & 7 other authors (2001). toxB gene on pO157 of enterohemorrhagic Escherichia coli is required for full epithelial cell adherence phenotype. Infect Immun 69, 6660-6669.
81. Torres, A. G. & Kaper, J. B. (2003). Multiple elements controlling the adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect Immun 71, 4985-4995.
82. Torres, A. G., Giron, J. A., Perna, N. T., Burland, V., Blattner, F. R., Avelino-Flores, F. & Kaper, J. B. (2002). Identification and characterization of lpfABCC′DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70, 5416-5427.
83. Toyotome, T., Suzuki, T., Kuwae, A., Nonaka, T., Fukuda, H., Imajoh-Ohmi, S., Toyofuku, T., Hori, M. & Sasakawa, C. (2001 . Shigella protein IpaH(9.8) is secreted from bacteria within mammalian cells and transported to the nucleus. J Biol Chem 276, 32071-32079.
84. Tzipori, S., Karch, H., Wachsmuth, K. I., Robins-Browne, R. M., O'Brien, A. D., Lior, H., Cohen, M. I., Smithers, J. & Levine, M. M. (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.
85. Uhlich, G. A., Keen, J. E. & Elder, R. O. (2002). Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect Immun 70, 395-399.
86. Viswanathan, V. K., Koutsouris, A., Lukic, S., Pilkinton, M., Simonovic, I., Simonovic, M. & Hecht, G. (2004). Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 72, 3218-3227.
87. Volf, J., Sevcik, M., Havlickova, H., Sisak, F., Damborsky, J. & Rychlik, I. (2002). Role of SdiA in Salmonella enterica serovar Typhimurium physiology and virulence. Arch Microbiol 178, 94-101.
88. Wachter, C., Beinke, C., Mattes, M. & Schmidt, M. A. (1999). Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol Microbiol 31, 1695-1707.
89. West, N. P., Sansonetti, P. J., Frankel, G. & Tang, C. M. (2003). Finding your niche: what has been learnt from STM studies on GI colonization. Trends Microbiol 11, 338-344.
90. WHO (1997). Prevention and Control of Enterohaemorrhagic Escherichia coli (EHEC) Infections. Report of a WHO consultation, Geneva, Switzerland.
91. Woodward, M. J., Best A., Sprigings, K. A. & 7 other authors (2003). Non-toxigenic Escherichia coli O157:H7 strain NCTC12900 causes attaching-effacing lesions and eae-dependent persistence in weaned sheep. Int J Med Microbiol 293, 299-308.
92. Wray, C., McLaren, I. M., Randall, L. P. & Pearson, G. R. (2000). Natural and experimental infection of normal cattle with Escherichia coli O157. Vet Rec 147, 65-68.