1887

Abstract

Enterohaemorrhagic (EHEC) cause acute gastroenteritis in humans that may be complicated by life-threatening systemic sequelae. The predominant EHEC serotype affecting humans in the UK and North America is O157 : H7 and infections are frequently associated with contact with ruminant faeces. Strategies to reduce the carriage of EHEC in ruminants are expected to lower the incidence of human EHEC infections; however, the molecular mechanisms underlying persistence of EHEC in ruminants are poorly understood. This paper reports the first comprehensive survey for EHEC factors mediating colonization of the bovine intestines by using signature-tagged transposon mutagenesis. Seventy-nine O157 : H7 mutants impaired in their ability to colonize calves were isolated and 59 different genes required for intestinal colonization were identified by cloning and sequencing of the transposon insertion sites. Thirteen transposon insertions were clustered in the locus of enterocyte effacement (LEE), which encodes a type III protein secretion system required for the formation of attaching and effacing lesions on intestinal epithelia. A putative structural component of the apparatus (EscN) is essential for intestinal colonization; however, the type III secreted effector protein Map plays only a minor role. Other Type III secretion-associated genes were implicated in colonization of calves by O157 : H7, including (), which encodes the non-LEE-encoded type III secreted effector NleD and the closely related () and () genes which encode homologues of IpaH proteins. We also identified a novel fimbrial locus required for intestinal colonization in calves by O157 : H7 (-; -/locus 8) and demonstrated that a mutant harbouring a deletion of the putative major fimbrial subunit gene is rapidly out-competed by the parent strain in co-infection studies. Our data provide valuable new information for the development of intervention strategies.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27448-0
2004-11-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/11/mic1503631.html?itemId=/content/journal/micro/10.1099/mic.0.27448-0&mimeType=html&fmt=ahah

References

  1. Ammon, A. ( 1997; ). Surveillance of enterohaemorrhagic Escherichia coli (EHEC) infections and haemolytic uraemic syndrome (HUS) in Europe. Euro Surveill 2, 91–96.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  3. Bettelheim, K. A. ( 2000; ). The role of non-O157 VTEC. Symp Ser Soc Appl Microbiol 29, 38S–50S.
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  19. Dytoc, M., Soni, R., Cockerill, F., 3rd, De Azavedo, J., Louie, M., Brunton, J. & Sherman, P. ( 1993; ). Multiple determinants of verotoxin-producing Escherichia coli O157 : H7 attachment-effacement. Infect Immun 61, 3382–3391.
    [Google Scholar]
  20. Ebel, F., Podzadel, T., Rohde, M., Kresse, A. U., Kramer, S., Deibel, 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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  31. Hoey, D. E., Currie, C., Else, R. W., Nutikka, A., Lingwood, C. A., Gally, 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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  39. Kenny, B. & Jepson, M. ( 2000; ). Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2, 579–590.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  55. Nataro, J. P. & Kaper, J. B. ( 1998; ). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142–201.
    [Google Scholar]
  56. Naylor, S. W., Low, J. C., Besser, T. E., Mahajan, A., Gunn, G. J., Pearce, M. C., McKendrick, I. J., Smith, D. G. & Gally, 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.[CrossRef]
    [Google Scholar]
  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 epithelial cells. Mol Microbiol 35, 275–288.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  59. Orskov, F., Orskov, I. & Villar, J. A. ( 1987; ). Cattle as a reservoir of verotoxin-producing Escherichia coli O157 : H7. Lancet 10, 276.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  62. Paton, J. C. & Paton, A. W. ( 1998; ). Pathogenesis and diagnosis of Shiga-toxin producing Escherichia coli infections. Clin Microbiol Rev 11, 450–479.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  71. Sherman, P., Cockerill, F., 3rd, Soni, R. & Brunton, J. ( 1991; ). Outer membranes are competitive inhibitors of Escherichia coli O157 : H7 adherence to epithelial cells. Infect Immun 59, 890–899.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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 lpfABCCDE, a fimbrial operon of enterohemorrhagic Escherichia coli O157 : H7. Infect Immun 70, 5416–5427.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27448-0
Loading
/content/journal/micro/10.1099/mic.0.27448-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error