1887

Microbiology Society logo

Volume 153, Issue 3

Human intestinal tissue tropism in O157 : H7 – initial colonization of terminal ileum and Peyer's patches and minimal colonic adhesion Free

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.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): A/E, attaching/effacing , D4, fourth part of duodenum , EAEC, enteroaggregative Escherichia coli , EHEC, enterohaemorrhagic Escherichia coli , EPEC, enteropathogenic Escherichia coli , FAE, follicle-associated epithelium , IVOC, in vitro organ culture , LEE, locus of enterocyte effacement , Lpf, long polar fimbriae , PP, Peyer's patches , REPEC, rabbit enteropathogenic E coli , SEM, scanning electron microscopy and Stx, Shiga toxin
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/003178-0
2007-03-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/3/794.html?itemId=/content/journal/micro/10.1099/mic.0.2006/003178-0&mimeType=html&fmt=ahah

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., Kaper J. B., Donohue-Rolfe A., de Montigny L. 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]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/003178-0
Loading
Human intestinal tissue tropism in Escherichia coli O157 : H7 – initial colonization of terminal ileum and Peyer's patches and minimal colonic adhesion ex vivo
Microbiology 153, 794 (2007); https://doi.org/10.1099/mic.0.2006/003178-0
/content/journal/micro/10.1099/mic.0.2006/003178-0
/content/journal/micro/10.1099/mic.0.2006/003178-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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