A subset of mucosa-associated isolates from patients with colon cancer, but not Crohn's disease, share pathogenicity islands with urinary pathogenic Free

Abstract

Adherent and invasive mucosa-associated have been implicated in the pathogenesis of colon cancer and inflammatory bowel diseases. It has been reported that such isolates share features of extraintestinal (ExPEC) and particularly uropathogenic (UPEC). We used suppression subtractive hybridization (SSH) to subtract the genome of K-12 from that of a colon cancer mucosal isolate. Of the subtracted sequences, 53 % were present in the genomes of one or more of three sequenced UPEC strains but absent from the genome of an enterohaemorrhagic (EHEC) strain. Of the subtracted sequences, 80 % matched at least one UPEC genome, whereas only 4 % were absent from the UPEC genomes but present in the genome of the EHEC strain. A further genomic subtraction against the UPEC strain 536 enriched for sequences matching mobile genetic elements, other ExPEC strains, and other UPEC strains or commensals, rather than strains associated with gastrointestinal disease. We analysed the distribution of selected subtracted sequences and UPEC-associated pathogenicity islands (PAIs) amongst a panel of mucosa-associated isolated from colonoscopic biopsies of patients with colon cancer, patients with Crohn's disease and controls. This enabled us to identify a group of isolates from colon cancer (30–40 %) carrying multiple genes previously categorized as UPEC-specific and implicated in virulence.

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2008-02-01
2024-03-28
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References

  1. Barnich N., Bringer M. A., Claret L., Darfeuille-Michaud A. 2004; Involvement of lipoprotein NlpI in the virulence of adherent invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 72:2484–2493
    [Google Scholar]
  2. Bergsten G., Samuelsson M., Wullt B., Leijonhufvud I., Fischer H., Svanborg C. 2004; PapG-dependent adherence breaks mucosal inertia and triggers the innate host response. J Infect Dis 189:1734–1742
    [Google Scholar]
  3. Bidet P., Metais A., Mahjoub-Messai F., Durand L., Dehem M., Aujard Y., Bingen E., Nassif X., Bonacorsi S. 2007; Detection and identification by PCR of a highly virulent phylogenetic subgroup among extraintestinal pathogenic Escherichia coli B2 strains. Appl Environ Microbiol 73:2373–2377
    [Google Scholar]
  4. Bringer M. A., Glasser A. L., Tung C. H., Meresse S., Darfeuille-Michaud A. 2006; The Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 replicates in mature phagolysosomes within J774 macrophages. Cell Microbiol 8:471–484
    [Google Scholar]
  5. Brzuszkiewicz E., Bruggemann H., Liesegang H., Emmerth M., Olschlager T., Nagy G., Albermann K., Wagner C., Buchrieser C. other authors 2006; How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A 103:12879–12884
    [Google Scholar]
  6. Chen S. L., Hung C. S., Xu J., Reigstad C. S., Magrini V., Sabo A., Blasiar D., Bieri T., Meyer R. R. other authors 2006; Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli : a comparative genomics approach. Proc Natl Acad Sci U S A 103:5977–5982
    [Google Scholar]
  7. Clermont O., Bonacorsi S., Bingen E. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558
    [Google Scholar]
  8. Darfeuille-Michaud A., Neut C., Barnich N., Lederman E., Di Martino P., Desreumaux P., Gambiez L., Joly B., Cortot A., Colombel J. F. 1998; Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115:1405–1413
    [Google Scholar]
  9. Darfeuille-Michaud A., Boudeau J., Bulois P., Neut C., Glasser A. L., Barnich N., Bringer M. A., Swidsinski A., Beaugerie L., Colombel J. F. 2004; High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127:412–421
    [Google Scholar]
  10. Dobrindt U., Blum-Oehler G., Nagy G., Schneider G., Johann A., Gottschalk G., Hacker J. 2002; Genetic structure and distribution of four pathogenicity islands (PAI I536 to PAI IV536) of uropathogenic Escherichia coli strain 536. Infect Immun 70:6365–6372
    [Google Scholar]
  11. Dobrindt U., Hochhut B., Hentschel U., Hacker J. 2004; Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424
    [Google Scholar]
  12. Ewers C., Li G., Wilking H., Kiebetaling S., Alt K., Antao E. M., Laturnus C., Diehl I., Glodde S. other authors 2007; Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli : how closely related are they?. Int J Med Microbiol 297:163–176
    [Google Scholar]
  13. Gal-Mor O., Finlay B. B. 2006; Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8:1707–1719
    [Google Scholar]
  14. Greten F. R., Eckmann L., Greten T. F., Park J. M., Li Z. W., Egan L. J., Kagnoff M. F., Karin M. 2004; IKK β links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285–296
    [Google Scholar]
  15. Guyer D. M., Kao J. S., Mobley H. L. 1998; Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and catheter-associated bacteriuria and from fecal samples. Infect Immun 66:4411–4417
    [Google Scholar]
  16. Hejnova J., Dobrindt U., Nemcova R., Rusniok C., Bomba A., Frangeul L., Hacker J., Glaser P., Sebo P., Buchrieser C. 2005; Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83 : K24 : H31). Microbiology 151:385–398
    [Google Scholar]
  17. Hochhut B., Wilde C., Balling G., Middendorf B., Dobrindt U., Brzuszkiewicz E., Gottschalk G., Carniel E., Hacker J. 2006; Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol Microbiol 61:584–595
    [Google Scholar]
  18. Hope M. E., Hold G. L., Kain R., El Omar E. M. 2005; Sporadic colorectal cancer – role of the commensal microbiota. FEMS Microbiol Lett 244:1–7
    [Google Scholar]
  19. Houdouin V., Bonacorsi S., Bidet P., Bingen-Bidois M., Barraud D., Bingen E. 2006; Phylogenetic background and carriage of pathogenicity island-like domains in relation to antibiotic resistance profiles among Escherichia coli urosepsis isolates. J Antimicrob Chemother 58:748–751
    [Google Scholar]
  20. Johnson J. R., Stell A. L. 2000; Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272
    [Google Scholar]
  21. Johnson J. R., Brown J. J., Maslow J. N. 1998; Clonal distribution of the three alleles of the Gal( α 1–4)Gal-specific adhesin gene papG among Escherichia coli strains from patients with bacteremia. J Infect Dis 177:651–661
    [Google Scholar]
  22. Johnson J. R., Scheutz F., Ulleryd P., Kuskowski M. A., O'Bryan T. T., Sandberg T. 2005; Phylogenetic and pathotypic comparison of concurrent urine and rectal Escherichia coli isolates from men with febrile urinary tract infection. J Clin Microbiol 43:3895–3900
    [Google Scholar]
  23. Johnson T. J., Kariyawasam S., Wannemuehler Y., Mangiamele P., Johnson S. J., Doetkott C., Skyberg J. A., Lynne A. M., Johnson J. R., Nolan L. K. 2007; The genome sequence of avian pathogenic Escherichia coli strain O1 : K1 : H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189:3228–3236
    [Google Scholar]
  24. Kaper J. B., Nataro J. P., Mobley H. L. 2004; Pathogenic Escherichia coli . Nat Rev Microbiol 2:123–140
    [Google Scholar]
  25. Klemm P., Schembri M. A. 2000; Bacterial adhesins: function and structure. Int J Med Microbiol 290:27–35
    [Google Scholar]
  26. Kotlowski R., Bernstein C. N., Sepehri S., Krause D. O. 2007; High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669–675
    [Google Scholar]
  27. Liu Y., van Kruiningen H. J., West A. B., Cartun R. W., Cortot A., Colombel J. F. 1995; Immunocytochemical evidence of Listeria, Escherichia coli , and Streptococcus antigens in Crohn's disease. Gastroenterology 108:1396–1404
    [Google Scholar]
  28. Lloyd A. L., Rasko D. A., Mobley H. L. 2007; Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli . J Bacteriol 189:3532–3546
    [Google Scholar]
  29. Mager D. L. 2006; Bacteria and cancer: cause, coincidence or cure? A review. J Transl Med 4:14
    [Google Scholar]
  30. Manson J. M., Gilmore M. S. 2006; Pathogenicity island integrase cross-talk: a potential new tool for virulence modulation. Mol Microbiol 61:555–559
    [Google Scholar]
  31. Martin H. M., Campbell B. J., Hart C. A., Mpofu C., Nayar M., Singh R., Englyst H., Williams H. F., Rhodes J. M. 2004; Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 127:80–93
    [Google Scholar]
  32. Meconi S., Vercellone A., Levillain F., Payre B., Al Saati T., Capilla F., Desreumaux P., Darfeuille-Michaud A., Altare F. 2007; Adherent-invasive Escherichia coli isolated from Crohn's disease patients induce granulomas in vitro . Cell Microbiol 9:1252–1261
    [Google Scholar]
  33. Middendorf B., Hochhut B., Leipold K., Dobrindt U., Blum-Oehler G., Hacker J. 2004; Instability of pathogenicity islands in uropathogenic Escherichia coli 536. J Bacteriol 186:3086–3096
    [Google Scholar]
  34. Mylonaki M., Rayment N. B., Rampton D. S., Hudspith B. N., Brostoff J. 2005; Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis 11:481–487
    [Google Scholar]
  35. Oelschlaeger T. A., Dobrindt U., Hacker J. 2002a; Pathogenicity islands of uropathogenic E. coli and the evolution of virulence. Int J Antimicrob Agents 19:517–521
    [Google Scholar]
  36. Oelschlaeger T. A., Dobrindt U., Hacker J. 2002b; Virulence factors of uropathogens. Curr Opin Urol 12:33–38
    [Google Scholar]
  37. Perna N. T., Plunkett G. III, Burland V., Mau B., Glasner J. D., Rose D. J., Mayhew G. F., Evans P. S., Gregor J. other authors 2001; Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature 409:529–533
    [Google Scholar]
  38. Rasko D. A., Phillips J. A., Li X., Mobley H. L. 2001; Identification of DNA sequences from a second pathogenicity island of uropathogenic Escherichia coli CFT073: probes specific for uropathogenic populations. J Infect Dis 184:1041–1049
    [Google Scholar]
  39. Rhodes J. M., Campbell B. J. 2002; Inflammation and colorectal cancer: IBD-associated and sporadic cancer compared. Trends Mol Med 8:10–16
    [Google Scholar]
  40. Rodriguez-Siek K. E., Giddings C. W., Doetkott C., Johnson T. J., Fakhr M. K., Nolan L. K. 2005; Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 151:2097–2110
    [Google Scholar]
  41. Rolhion N., Barnich N., Claret L., Darfeuille-Michaud A. 2005; Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 187:2286–2296
    [Google Scholar]
  42. Rolhion N., Carvalho F. A., Darfeuille-Michaud A. 2007; OmpC and the σ E regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol 63:1684–1700
    [Google Scholar]
  43. Ryan P., Kelly R. G., Lee G., Collins J. K., O'Sullivan G. C., O'Connell J., Shanahan F. 2004; Bacterial DNA within granulomas of patients with Crohn's disease – detection by laser capture microdissection and PCR. Am J Gastroenterol 99:1539–1543
    [Google Scholar]
  44. Sabaté M., Moreno E., Perez T., Andreu A., Prats G. 2006; Pathogenicity island markers in commensal and uropathogenic Escherichia coli isolates. Clin Microbiol Infect 12:880–886
    [Google Scholar]
  45. Schmidt H., Hensel M. 2004; Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17:14–56
    [Google Scholar]
  46. Schubert S., Rakin A., Heesemann J. 2004; The Yersinia high-pathogenicity island (HPI): evolutionary and functional aspects. Int J Med Microbiol 294:83–94
    [Google Scholar]
  47. Simpson K. W., Dogan B., Rishniw M., Goldstein R. E., Klaessig S., McDonough P. L., German A. J., Yates R. M., Russell D. G. other authors 2006; Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun 74:4778–4792
    [Google Scholar]
  48. Swidsinski A., Khilkin M., Kerjaschki D., Schreiber S., Ortner M., Weber J., Lochs H. 1998; Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 115:281–286
    [Google Scholar]
  49. Swidsinski A., Ladhoff A., Pernthaler A., Swidsinski S., Loening-Baucke V., Ortner M., Weber J., Hoffmann U., Schreiber S. other authors 2002; Mucosal flora in inflammatory bowel disease. Gastroenterology 122:44–54
    [Google Scholar]
  50. Welch R. A., Burland V., Plunkett G. III, Redford P., Roesch P., Rasko D., Buckles E. L., Liou S. R., Boutin A. other authors 2002; Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli . Proc Natl Acad Sci U S A 99:17020–17024
    [Google Scholar]
  51. Whitfield C., Roberts I. S. 1999; Structure, assembly and regulation of expression of capsules in Escherichia coli . Mol Microbiol 31:1307–1319
    [Google Scholar]
  52. Wullt B., Bergsten G., Connell H., Rollano P., Gebretsadik N., Hull R., Svanborg C. 2000; P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract. Mol Microbiol 38:456–464
    [Google Scholar]
  53. Wullt B., Bergsten G., Samuelsson M., Svanborg C. 2002; The role of P fimbriae for Escherichia coli establishment and mucosal inflammation in the human urinary tract. Int J Antimicrob Agents 19:522–538
    [Google Scholar]
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