1887

Abstract

Avian pathogenic (APEC) and uropathogenic (UPEC) establish infections in extraintestinal habitats of different hosts. As the diversity, epidemiological sources and evolutionary origins of extraintestinal pathogenic (ExPEC) are so far only partially defined, in the present study,100 APEC isolates and 202 UPEC isolates were compared by their content of virulence genes and phylogenetic groups. The two groups showed substantial overlap in terms of their serogroups, phylogenetic groups and virulence genotypes, including their possession of certain genes associated with large transmissible plasmids of APEC. In a chicken challenge model, both UPEC U17 and APEC E058 had similar LD, demonstrating that UPEC U17 had the potential to cause significant disease in poultry. To gain further information about the similarities between UPEC and APEC, the expression of 152 specific genes of UPEC U17 and APEC E058 in both a murine urinary tract infection (UTI) model and a chicken challenge model was compared with that of these strains grown statically to exponential phase in rich medium. It was found that in the same model (murine UTI or chicken challenge), various genes of UPEC U17 and APEC E058 showed a similar tendency of expression. Several iron-related genes were upregulated in the UTI model and/or chicken challenge model, indicating that iron acquisition is important for to survive in blood or the urinary tract. Based on these results, the potential for APEC to act as human UPEC or as a reservoir of virulence genes for UPEC should be considered. Further, this study compared the transcriptional profile of virulence genes among APEC and UPEC .

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2009-05-01
2019-10-15
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References

  1. Barnes, H. J., Vaillancourt, J. P. & Gross, W. B. ( 2003; ). Colibacillosis. In Diseases of Poultry, pp. 631–652. Edited by Y. M. Saif. Ames, IA: Iowa State University Press.
  2. Bonacorsi, S. P. P., Clermont, O., Tinsley, C., Gall, L. I., Beaudoin, J. C., Elion, J., Nassif, X. & Bingen, E. ( 2000; ). Identification of regions of the Escherichia coli chromosome specific for neonatal meningitis-associated strains. Infect Immun 68, 2096–2101.[CrossRef]
    [Google Scholar]
  3. Bullen, J. J., Rogers, H. J., Spalding, P. B. & Ward, C. G. ( 2005; ). Iron and infection: the heart of the matter. FEMS Immunol Med Microbiol 43, 325–330.[CrossRef]
    [Google Scholar]
  4. Burman, W. J., Breese, P. E., Murray, B. E., Singh, K. Y., Batal, H. A., Mackenzie, T. D., Ogle, J. W., Wilson, M. L., Reves, R. R. & Mehler, P. S. ( 2003; ). Conventional and molecular epidemiology of trimethoprim-sulfamethoxazole resistance among urinary Escherichia coli isolates. Am J Med 115, 358–364.[CrossRef]
    [Google Scholar]
  5. Chen, X. ( 2006; ). Biological characteristics of avian pathogenic Escherichia coli isolates in China and identification of their virulence-related genes. PhD thesis, Yangzhou University.
  6. Chen, X., Gao, S., Wang, X. Q., Jiao, X. A. & Liu, X. F. ( 2007; ). Identification of APEC genes expressed in vivo by selective capture of transcribed sequences. Wei Sheng Wu Xue Bao 47, 407–412.
    [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.[CrossRef]
    [Google Scholar]
  8. Dho, M. & Lafont, J. P. ( 1984; ). Adhesive properties and iron uptake ability in Escherichia coli lethal and nonlethal for chicks. Avian Dis 28, 1016–1025.[CrossRef]
    [Google Scholar]
  9. Dobrindt, U., Blum-Oehler, G., Hartsch, T., Gottschalk, G., Ron, E. Z., Funfstuck, R. & Hacker, J. ( 2001; ). S-fimbria-encoding determinant sfa (I) is located on pathogenicity island III(536) of uropathogenic Escherichia coli strain 536. Infect Immun 69, 4248–4256.[CrossRef]
    [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 I (536) to PAI IV (536)) of uropathogenic Escherichia coli strain 536. Infect Immun 70, 6365–6372.[CrossRef]
    [Google Scholar]
  11. Donnenberg, M. S. & Welch, R. ( 1996; ). Virulence determinants of uropathogenic Escherichia coli. In Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, pp. 135–174. Edited by H. L. T. Mobley & J. W. Warren. Washington, DC: American Society for Microbiology.
  12. Forbes, B. A., Sahm, D. F. & Weissfeld, A. S. ( 1998; ). Bailey and Scott's Diagnostic Microbiology. St Louis, MO: Mosby.
  13. Foxman, B., Barlow, R., D'Arcy, H., Gillespie, B. & Sobel, J. D. ( 2000; ). Urinary tract infection: self-reported incidence and associated costs. Ann Epidemiol 10, 509–515.[CrossRef]
    [Google Scholar]
  14. Hagan, E. C. & Mobley, H. L. ( 2007; ). Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection. Infect Immun 75, 3941–3949.[CrossRef]
    [Google Scholar]
  15. Hagberg, L., Engberg, I., Freter, R., Lam, J., Olling, S. & Eden, C. S. ( 1983; ). Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect Immun 40, 273–283.
    [Google Scholar]
  16. Haugen, B. J., Pellett, S., Redford, P., Hamilton, H. L., Roesch, P. L. & Welch, R. A. ( 2007; ). In vivo gene expression analysis identifies genes required for enhanced colonization of the mouse urinary tract by uropathogenic Escherichia coli strain CFT073 dsdA. Infect Immun 75, 278–289.[CrossRef]
    [Google Scholar]
  17. Huan, H. X. ( 2007; ). Construction of DNA chips composed of APEC, UPEC virulence and potential virulence genes and screening of distinct expressed genes in vivo and in vitro among virulence and potential virulence genes between APEC and UPEC by DNA microarray assay. PhD Thesis, Yangzhou University.
  18. Janben, T., Schwarz, C., Preikschat, P., Voss, M., Philipp, H. C. & Wieler, L. H. ( 2001; ). Virulence-associated genes in avian pathogenic Escherichia coli (APEC) isolated from internal organs of poultry having died from colibacillosis. Int J Med Microbiol 291, 371–378.[CrossRef]
    [Google Scholar]
  19. Johnson, J. R. ( 1991; ). Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4, 80–128.
    [Google Scholar]
  20. Johnson, J. R. & Russo, T. A. ( 2002; ). Uropathogenic Escherichia coli as agents of diverse non-urinary tract extraintestinal infections. J Infect Dis 186, 859–864.[CrossRef]
    [Google Scholar]
  21. 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.[CrossRef]
    [Google Scholar]
  22. Johnson, D. E., Lockatell, C. V., Russell, R. G., Hebel, J. R., Island, M. D., Stapleton, A., Stamm, W. E. & Warren, J. W. ( 1998; ). Comparison of Escherichia coli strains recovered from human cystitis and pyelonephritis infections in transurethrally challenged mice. Infect Immun 66, 3059–3065.
    [Google Scholar]
  23. Johnson, J. R., Delavari, P., Kuskowski, M. & Stell, A. L. ( 2001a; ). Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183, 78–88.[CrossRef]
    [Google Scholar]
  24. Johnson, J. R., Stell, A. L., Delavari, P., Murray, A. C., Kuskowski, M. & Gaastra, W. ( 2001b; ). Phylogenetic and pathotypic similarities between Escherichia coli isolates from urinary tract infections in dogs and extraintestinal infections in humans. J Infect Dis 183, 897–906.[CrossRef]
    [Google Scholar]
  25. Johnson, T. J., Giddings, C. W., Horne, S. M., Gibbs, P. S., Wooley, R. E., Skyberg, J., Olah, P., Kercher, R., Sherwood, J. S. & other authors ( 2002; ). Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate. Avian Dis 46, 342–352.[CrossRef]
    [Google Scholar]
  26. Johnson, J. R., Owens, K. L., Clabots, C. R., Weissman, S. J. & Cannon, S. B. ( 2006a; ). Phylogenetic relationships among clonal groups of extraintestinal pathogenic Escherichia coli as assessed by multi-locus sequence analysis. Microbes Infect 8, 1702–1713.[CrossRef]
    [Google Scholar]
  27. Johnson, T. J., Siek, K. E., Johnson, S. J. & Nolan, L. K. ( 2006b; ). DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 188, 745–758.[CrossRef]
    [Google Scholar]
  28. Kaper, J. B., Nataro, J. P. & Mobley, H. L. ( 2004; ). Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123–140.[CrossRef]
    [Google Scholar]
  29. Lawlor, M. S., O'Connor, C. & Miller, V. L. ( 2007; ). Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection. Infect Immun 75, 1463–1472.[CrossRef]
    [Google Scholar]
  30. Levy, S. B., FitzGerald, G. B. & Macone, A. B. ( 1976; ). Spread of antibiotic-resistant plasmids from chicken to chicken and from chicken to man. Nature 260, 40–42.[CrossRef]
    [Google Scholar]
  31. Linton, A. H., Howe, K., Bennett, P. M., Richmond, M. H. & Whiteside, E. J. ( 1977; ). The colonization of the human gut by antibiotic resistant Escherichia coli from chickens. J Appl Bacteriol 43, 465–469.[CrossRef]
    [Google Scholar]
  32. Mokady, D., Gophna, U. & Ron, E. Z. ( 2005; ). Extensive gene diversity in septicemic Escherichia coli strains. J Clin Microbiol 43, 66–73.[CrossRef]
    [Google Scholar]
  33. Moulin-Schouleur, M., Schouler, C., Tailliez, P., Kao, M. R., Bree, A., Germon, P., Oswald, E., Mainil, J., Blanco, M. & Blanco, J. ( 2006; ). Common virulence factors and genetic relationships between O18 : K1 : H7 Escherichia coli isolates of human and avian origin. J Clin Microbiol 44, 3484–3492.[CrossRef]
    [Google Scholar]
  34. Mulvey, M. A., Lopez-Boado, Y. S., Wilson, C. L., Roth, R., Parks, W. C., Heuser, J. & Hultgren, S. J. ( 1998; ). Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282, 1494–1497.[CrossRef]
    [Google Scholar]
  35. Oelschlaeger, T. A., Dobrindt, U. & Hacker, J. ( 2002; ). Virulence factors of uropathogens. Curr Opin Urol 12, 33–38.[CrossRef]
    [Google Scholar]
  36. Ojeniyi, A. A. ( 1989; ). Direct transmission of Escherichia coli from poultry to humans. Epidemiol Infect 103, 513–522.[CrossRef]
    [Google Scholar]
  37. Piatti, G., Mannini, A., Balistreri, M. & Schito, A. M. ( 2008; ). Virulence factors in urinary Escherichia coli strains: phylogenetic background and quinolone and fluoroquinolone resistance. J Clin Microbiol 46, 480–487.[CrossRef]
    [Google Scholar]
  38. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  39. 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.[CrossRef]
    [Google Scholar]
  40. Ron, E. Z. ( 2006; ). Host specificity of septicemic Escherichia coli: human and avian pathogens. Curr Opin Microbiol 9, 28–32.[CrossRef]
    [Google Scholar]
  41. Rosenow, C., Saxena, R. M., Durst, M. & Gingeras, T. R. ( 2001; ). Prokaryotic RNA preparation methods useful for high density array analysis: comparison of two approaches. Nucleic Acids Res 29, E112 [CrossRef]
    [Google Scholar]
  42. Runyen-Janecky, L. J., Reeves, S. A., Gonzales, E. G. & Payne, S. M. ( 2003; ). Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71, 1919–1928.[CrossRef]
    [Google Scholar]
  43. Salyers, A. A. & Whitt, D. D. ( 1994; ). Escherichia coli gastrointestinal infections. In Bacterial Pathogenesis: a Molecular Approach, pp. 190–204. Edited by A. A. Salyers & D. D. Whitt. Washington, DC: American Society for Microbiology.
  44. Skyberg, J. A., Horne, S. M., Giddings, C. W., Wooley, R. E., Gibbs, P. S. & Nolan, L. K. ( 2003; ). Characterizing avian Escherichia coli isolates with multiplex polymerase chain reaction. Avian Dis 47, 1441–1447.[CrossRef]
    [Google Scholar]
  45. Snyder, J. A., Haugen, B. J., Buckles, E. L., Lockatell, C. V. D., Johnson, E., Donnenberg, M. S., Welch, R. A. & Mobley, H. L. ( 2004; ). Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72, 6373–6381.[CrossRef]
    [Google Scholar]
  46. Snyder, J. A., Haugen, B. J., Lockatell, C. V., Maroncle, N., Hagan, E. C., Johnson, D. E., Welch, R. A. & Mobley, H. L. ( 2005; ). Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun 73, 7588–7596.[CrossRef]
    [Google Scholar]
  47. Song, G., Xiufan, L., Rukuan, Z., Xinan, J., Qiyi, W., Changxin, W., Yiming, T., Xiaobo, Z., Cong, L. & other authors ( 1999; ). The isolation and identification of pathogenic Escherichia coli isolates of chicken from some regions in China. Acta Vet Zootech Sin 30, 164–171.
    [Google Scholar]
  48. Sorsa, L. J., Dufke, S., Heesemann, J. & Schubert, S. ( 2003; ). Characterization of an iroBCDEN gene cluster on a transmissible plasmid of uropathogenic Escherichia coli: evidence for horizontal transfer of a chromosomal virulence factor. Infect Immun 71, 3285–3293.[CrossRef]
    [Google Scholar]
  49. Torres, A. G., Redford, P., Welch, R. A. & Payne, S. M. ( 2001; ). TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 69, 6179–6185.[CrossRef]
    [Google Scholar]
  50. van den Bogaard, A. E., Willems, R., London, N., Top, J. & Stobberingh, E. E. ( 2002; ). Antibiotic resistance of faecal enterococci in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 49, 497–505.[CrossRef]
    [Google Scholar]
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