1887

Abstract

Enterohaemorrhagic (EHEC) are an important cause of diarrhoeal and renal disease in man. Studies of a single prototypic O157 : H7 strain have shown tropism for follicle-associated epithelium (FAE) of distal ileal Peyer's patches without colonization of either small or large intestine. This study determined tropism in a range of Shiga toxin (Stx)-negative EHEC strains and looked for factors that might induce colonic colonization using human intestinal organ culture (IVOC). An FAE-restricted colonization was confirmed in two strains; four strains additionally colonized ileal villous surfaces, and adhesion to proximal small intestinal FAE was observed. All strains showed minimal adhesion to non-FAE regions of proximal small intestinal and to the transverse colon. Extensive large-bowel IVOC studies using three O157 : H7 strains, an O26 : H11 and an O103 : H2 strain, and tissue from caecum to rectum found colonization and attaching/effacing lesion formation in only 4 of 113 (3.5 %) IVOCs. Colonic adhesion was not enhanced by altering the IVOC technique or environment. Co-incubation of O157 : H7-infected ileal FAE with colonic samples enhanced colonic colonization, producing a novel, non-intimate adhesive phenotype. Thus, in the initial stages of colonization Stx-negative EHEC preferentially infect FAE and villi of the terminal ileal region ; colonic colonization is infrequently observed as an initial event but may represent a subsequent stage of infection.

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2007-03-01
2019-11-21
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References

  1. Adu-Bobie, J., Frankel, G., Bain, C., Goncalves, A. G., Trabulsi, L. R., Douce, G., Knutton, S. & Dougan, G. ( 1998; ). Detection of intimins α, β, γ, and δ, four intimin derivatives expressed by attaching and effacing microbial pathogens. J Clin Microbiol 36, 662–668.
    [Google Scholar]
  2. Baumler, A. J., Tsolis, R. M. & Heffron, F. ( 1996; ). The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. Proc Natl Acad Sci U S A 93, 279–283.[CrossRef]
    [Google Scholar]
  3. Cantey, J. R. & Inman, L. R. ( 1981; ). Diarrhea due to Escherichia coli strain RDEC-1 in the rabbit: the Peyer's patch as the initial site of attachment and colonization. J Infect Dis 143, 440–446.[CrossRef]
    [Google Scholar]
  4. 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]
  5. Cornes, J. S. ( 1965; ). Number, size and distribution of Peyer's patches in the human small intestine. Part II. The effect of age on Peyer's patches. Gut 6, 230–233.[CrossRef]
    [Google Scholar]
  6. Dean-Nystrom, E. A., Bosworth, B. T. & Moon, H. W. ( 1997; ). Pathogenesis of O157 : H7 Escherichia coli infection in neonatal calves. Adv Exp Med Biol 412, 47–51.
    [Google Scholar]
  7. DuPont, H. L., Levine, M. M., Hornick, R. B. & Formal, S. B. ( 1989; ). Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 159, 1126–1128.[CrossRef]
    [Google Scholar]
  8. Feng, P., Dey, M., Abe, A. & Takeda, T. ( 2001; ). Isogenic strain of Escherichia coli O157 : H7 that has lost both Shiga toxin 1 and 2 genes. Clin Diagn Lab Immunol 8, 711–717.
    [Google Scholar]
  9. Fitzhenry, R. J., Pickard, D. J., Hartland, E. L., Reece, S., Dougan, G., Phillips, A. D. & Frankel, G. ( 2002a; ). Intimin type influences the site of human intestinal mucosal colonisation by enterohaemorrhagic Escherichia coli O157 : H7. Gut 50, 180–185.[CrossRef]
    [Google Scholar]
  10. Fitzhenry, R. J., Reece, S., Trabulsi, L. R., Heuschkel, R., Murch, S., Thomson, M., Frankel, G. & Phillips, A. D. ( 2002b; ). Tissue tropism of enteropathogenic Escherichia coli strains belonging to the O55 serogroup. Infect Immun 70, 4362–4368.[CrossRef]
    [Google Scholar]
  11. Fitzhenry, R. J., Stevens, M. P., Jenkins, C., Wallis, T. S., Heuschkel, R., Murch, S., Thomson, M., Frankel, G. & Phillips, A. D. ( 2003; ). Human intestinal tissue tropism of intimin epsilon O103 Escherichia coli. FEMS Microbiol Lett 218, 311–316.[CrossRef]
    [Google Scholar]
  12. Fitzhenry, R. J., Dahan, S., Torres, A. G., Chong, Y., Heuschkel, R., Murch, S., Thomson, M., Kaper, J. B., Frankel, G. & other authors ( 2006; ). Long polar fimbriae and tissue tropism in Escherichia coli O157 : H7. Microbes Infect 8, 1741–1749.[CrossRef]
    [Google Scholar]
  13. Frankel, G., Phillips, A. D., Rosenshine, I., Dougan, G., Kaper, J. B. & Knutton, S. ( 1998; ). Enteropathogenic and enterohemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30, 911–921.[CrossRef]
    [Google Scholar]
  14. Gally, D. L., Naylor, S. W., Low, J. C., Gunn, G. J., Synge, B. A., Pearce, M. C., Donachie, W. & Besser, T. E. ( 2003; ). Colonisation site of E. coli O157 in cattle. Vet Rec 152, 307.
    [Google Scholar]
  15. Gamage, S. D., Strasser, J. E., Chalk, C. L. & Weiss, A. A. ( 2003; ). Nonpathogenic Escherichia coli can contribute to the production of Shiga toxin. Infect Immun 71, 3107–3115.[CrossRef]
    [Google Scholar]
  16. Griffin, P. M., Olmstead, L. C. & Petras, R. E. ( 1990; ). Escherichia coli 0157 : H7-associated colitis. A clinical and histological study of 11 cases. Gastroenterology 99, 142–149.
    [Google Scholar]
  17. Hayashi, T., Makino, K., Ohnishi, M., Kurokawa, K., Ishii, K., Yokoyama, K., Han, C. G., Ohtsubo, E., Nakayama, K. & other authors ( 2001; ). Complete genome sequence of enterohemorrhagic Escherichia coli O157 : H7 and genomic comparison with a laboratory strain K-12. DNA Res 8, 11–22.[CrossRef]
    [Google Scholar]
  18. Heczko, U., Abe, A. & Finlay, B. B. ( 2000; ). In vivo interactions of rabbit enteropathogenic Escherichia coli O103 with its host: an electron microscopic and histopathologic study. Microbes Infect 2, 5–16.[CrossRef]
    [Google Scholar]
  19. Hicks, S., Candy, D. C. & Phillips, A. D. ( 1996; ). Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun 64, 4751–4760.
    [Google Scholar]
  20. Hicks, S., Frankel, G., Kaper, J. B., Dougan, G. & Phillips, A. D. ( 1998; ). Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect Immun 66, 1570–1578.
    [Google Scholar]
  21. Islam, D., Bandholtz, L., Nilsson, J., Wigzell, H., Christensson, B., Agerberth, B. & Gudmundsson, G. ( 2001; ). Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med 7, 180–185.[CrossRef]
    [Google Scholar]
  22. Jacewicz, M. S., Acheson, D. W., Binion, D. G., West, G. A., Lincicome, L. L., Fiocchi, C. & Keusch, G. T. ( 1999; ). Responses of human intestinal microvascular endothelial cells to Shiga toxins 1 and 2 and pathogenesis of hemorrhagic colitis. Infect Immun 67, 1439–1444.
    [Google Scholar]
  23. Jenkins, C., Lawson, A. J., Cheasty, T., Willshaw, G. A., Wright, P., Dougan, G., Frankel, G. & Smith, H. R. ( 2003; ). Subtyping intimin genes from enteropathogenic Escherichia coli associated with outbreaks and sporadic cases in the United Kingdom and Eire. Mol Cell Probes 17, 149–156.[CrossRef]
    [Google Scholar]
  24. Jerse, A. E., Yu, J., Tall, B. D. & Kaper, J. B. ( 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 U S A 87, 7839–7843.[CrossRef]
    [Google Scholar]
  25. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C. & Steele, B. T. ( 1983; ). Escherichia coli cytotoxin, haemolytic uremic syndrome, and haemorrhagic colitis. Lancet ii, 1299–1300.
    [Google Scholar]
  26. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C., Arbus, G. S. & Lior, H. ( 1985; ). The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis 151, 775–782.[CrossRef]
    [Google Scholar]
  27. Kelly, J. K., Pai, C. H., Jadusingh, I. H., Macinnis, M. L., Shaffer, E. A. & Hershfield, N. B. ( 1987; ). The histopathology of rectosigmoid biopsies from adults with bloody diarrhea due to verotoxin-producing Escherichia coli. Am J Clin Pathol 88, 78–82.
    [Google Scholar]
  28. Knutton, S., Lloyd, D. R. & McNeish, A. S. ( 1987; ). Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun 55, 69–77.
    [Google Scholar]
  29. Knutton, S., Baldwin, T., Williams, P. H. & McNeish, A. S. ( 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.
    [Google Scholar]
  30. Lewis, D. C., Walker-Smith, J. A. & Phillips, A. D. ( 1987; ). Polymorphonuclear neutrophil leucocytes in childhood Crohn's disease: a morphological study. J Pediatr Gastroenterol Nutr 6, 430–438.[CrossRef]
    [Google Scholar]
  31. Li, Z., Bell, C., Buret, A., Robins-Browne, R., Stiel, D. & O'Loughlin, E. ( 1993; ). The effect of enterohemorrhagic Escherichia coli O157 : H7 on intestinal structure and solute transport in rabbits. Gastroenterology 104, 467–474.
    [Google Scholar]
  32. Mariani-Kurkdjian, P., Denamur, E., Milon, A., Picard, B., Cave, H., Lambert-Zechovsky, N., Loirat, C., Goullet, P., Sansonetti, P. J. & other authors ( 2001; ). Identification of a clone of Escherichia coli O103 : H2 as a potential agent of hemolytic uremic syndrome in France. J Clin Microbiol 31, 296–301.
    [Google Scholar]
  33. Nataro, J. P. & Kaper, J. B. ( 1998; ). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142–201.
    [Google Scholar]
  34. Nataro, J. P., Deng, Y., Cookson, S., Cravioto, A., Savarino, S. J., Guers, L. D., Levine, M. M. & Tacket, C. O. ( 1995; ). Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis 171, 465–468.[CrossRef]
    [Google Scholar]
  35. Oswald, E., Schmidt, H., Morabito, S., Karch, H., Marches, O. & Caprioli, A. ( 2000; ). Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect Immun 68, 64–71.[CrossRef]
    [Google Scholar]
  36. Phillips, A. D. & Frankel, G. ( 2000; ). Intimin-mediated tissue specificity in enteropathogenic Escherichia coli interaction with human intestinal organ cultures. J Infect Dis 181, 1496–1500.[CrossRef]
    [Google Scholar]
  37. Phillips, A. D., Navabpour, S., Hicks, S., Dougan, G., Wallis, T. & Frankel, G. ( 2000; ). Enterohaemorrhagic Escherichia coli O157 : H7 target Peyer's patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut 47, 377–381.[CrossRef]
    [Google Scholar]
  38. Robinson, C. M., Sinclair, J. F., Smith, M. J. & O'Brien, A. D. ( 2006; ). Shiga toxin of enterohemorrhagic Escherichia coli type O157 : H7 promotes intestinal colonization. Proc Natl Acad Sci U S A 103, 9667–9672.[CrossRef]
    [Google Scholar]
  39. Rothbaum, R. J., McAdams, A. J., Giannella, R. & Partin, J. C. ( 1982; ). A clinicopathological study of enterocyte adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology 83, 441–454.
    [Google Scholar]
  40. Schuller, S., Frankel, G. & Phillips, A. D. ( 2004; ). Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell Microbiol 6, 289–301.[CrossRef]
    [Google Scholar]
  41. Slutsker, L., Ries, A. A., Greene, K. D., Wells, J. G., Hutwagner, L. & Griffin, P. M. ( 1997; ). Escherichia coli O157 : H7 diarrhea in the United States: clinical and epidemiologic features. Ann Intern Med 126, 505–513.[CrossRef]
    [Google Scholar]
  42. Sperandio, V., Mellies, J. L., Nguyen, W., Shin, S. & Kaper, J. B. ( 1999; ). Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96, 15196–15201.[CrossRef]
    [Google Scholar]
  43. Tarr, P. I. ( 1995; ). Escherichia coli O157 : H7: clinical, diagnostic, and epidemiological aspects of human infection. Clin Infect Dis 20, 1–10.[CrossRef]
    [Google Scholar]
  44. 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.[CrossRef]
    [Google Scholar]
  45. Tzipori, S., Wachsmuth, I. K., Chapman, C., Birden, R., Brittingham, J., Jackson, C. & Hogg, J. ( 1986; ). The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157 : H7 in gnotobiotic piglets. J Infect Dis 154, 712–716.[CrossRef]
    [Google Scholar]
  46. Tzipori, S., Karch, H., Wachsmuth, I. K., Robins-Browne, R. M., O'Brien, A. D., Lior, H., Cohen, M. L., Smithers, J. & Levine, M. M. ( 1987; ). Role of a 60-megadalton plasmid and shiga-like toxins in the pathogenesis of enterohaemorrhagic Escherichia coli O157 : H7 in gnotobiotic piglets. Infect Immun 55, 3117–3125.
    [Google Scholar]
  47. Tzipori, S., Gunzer, F., Donnenberg, M. S., de Montigny, L., Kaper, J. B. & Donohue-Rolfe, A. ( 1995; ). The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63, 3621–3627.
    [Google Scholar]
  48. Von Moll, L. K. & Cantey, J. R. ( 1997; ). Peyer's patch adherence of enteropathogenic Escherichia coli strains in rabbits. Infect Immun 65, 3788–3793.
    [Google Scholar]
  49. Wiles, S., Clare, S., Harker, J., Huett, A., Young, D., Dougan, G. & Frankel, G. ( 2004; ). Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6, 963–972.[CrossRef]
    [Google Scholar]
  50. Wiles, S., Dougan, G. & Frankel, G. ( 2005; ). Emergence of a ‘hyperinfectious' bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol 7, 1163–1172.[CrossRef]
    [Google Scholar]
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