1887

Abstract

The presence of , a gene encoding a known virulence factor of strains responsible for neonatal meningitis in humans, was investigated in the genome of 213 avian pathogenic (APEC) strains and 55 non-pathogenic strains of avian origin. Fifty-three strains were found to be , all of which belonged to the APEC group. The gene is therefore positively linked to the pathogenicity of strains (<0·0001). Analysis of the serogroup of strains revealed a positive association of with serogroups O18, O88 and O2. On the contrary, only 1/59 O78 strains are , indicating a negative association of with this serogroup (<0·0001). The role of in the virulence of the APEC strain BEN 2908 was investigated by constructing an mutant. Challenge assays on 3-week-old chickens showed a reduced virulence for the mutant. Furthermore, the APEC strain BEN 2908 was able to invade brain microvascular epithelial cells, this invasion being significantly reduced upon inactivation of . Altogether, these results suggest a role of in the pathogenicity of some APEC strains and confirm the close relationship between APEC and other human extraintestinal pathogenic isolates.

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2005-04-01
2019-10-15
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References

  1. Achtman, M., Heuzenroeder, M. W., Kusecek, B. & 8 other authors ( 1986; ). Clonal analysis of Escherichia coli O2 : K1 isolated from diseased humans and animals. Infect Immun 51, 268–276.
    [Google Scholar]
  2. Bahrani-Mougeot, F. K., Buckles, E. L., Lockatell, C. V., Hebel, J. R., Johnson, D. E., Tang, C. M. & Donnenberg, M. S. ( 2002; ). Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol Microbiol 45, 1079–1093.[CrossRef]
    [Google Scholar]
  3. Bingen, E., Bonacorsi, S., Brahimi, N., Denamur, E. & Elion, J. ( 1997; ). Virulence patterns of Escherichia coli K1 strains associated with neonatal meningitis. J Clin Microbiol 1997, 2981–2982.
    [Google Scholar]
  4. Binns, M. M., Davies, D. L. & Hardy, K. G. ( 1979; ). Cloned fragments of the plasmid ColV,I-K94 specifying virulence and serum resistance. Nature 279, 778–781.[CrossRef]
    [Google Scholar]
  5. Blanco, J. E., Blanco, M., Mora, A. & Blanco, J. ( 1997; ). Production of toxins (enterotoxins, verotoxins, and necrotoxins) and colicins by Escherichia coli strains isolated from septicemic and healthy chickens: relationship with in vivo pathogenicity. J Clin Microbiol 35, 2953–2957.
    [Google Scholar]
  6. Blanco, J., Blanco, M., Mora, A., Jansen, W., Garcia, V., Vazquez, M. & Blanco, J. ( 1998; ). Serotypes of Escherichia coli isolated from septicaemic chickens in Galicia (northwest Spain). Vet Microbiol 61, 229–235.[CrossRef]
    [Google Scholar]
  7. Chérifi, A., Contrepois, M., Picard, B., Goullet, P., Ørskov, I. & Ørskov, F. ( 1994; ). Clonal relationships among Escherichia coli serogroup O78 isolates from human and animal infections. J Clin Microbiol 32, 1197–1202.
    [Google Scholar]
  8. Delicato, E. R., de Brito, B. G., Gaziri, L. C. & Vidotto, M. C. ( 2003; ). Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis. Vet Microbiol 94, 97–103.[CrossRef]
    [Google Scholar]
  9. Dho-Moulin, M. & Fairbrother, J. M. ( 1999; ). Avian pathogenic Escherichia coli (APEC). Vet Res 30, 299–316.
    [Google Scholar]
  10. Dho-Moulin, M. & Lafont, J.-P. ( 1982; ). Escherichia coli colonization of the trachea in poultry: comparison of virulent and avirulent strains in gnotoxenic chickens. Avian Dis 26, 787–797.[CrossRef]
    [Google Scholar]
  11. Donnenberg, M. S. & Kaper, J. B. ( 1991; ). Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59, 4310–4317.
    [Google Scholar]
  12. Dozois, C. M., Fairbrother, J. M., Harel, J. & Bosse, M. ( 1992; ). pap-and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infect Immun 60, 2648–2656.
    [Google Scholar]
  13. Dozois, C. M., Harel, J. & Fairbrother, J. M. ( 1996; ). P-fimbriae-producing septicaemic Escherichia coli from poultry possess fel-related gene clusters whereas pap-hybridizing P-fimbriae-negative strains have partial or divergent P fimbrial gene clusters. Microbiology 142, 2759–2766.[CrossRef]
    [Google Scholar]
  14. Dozois, C. M., Dho-Moulin, M., Bree, A., Fairbrother, J. M., Desautels, C. & Curtiss, R., 3rd ( 2000; ). Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the Tsh genetic region. Infect Immun 68, 4145–4154.[CrossRef]
    [Google Scholar]
  15. Gunther, I. N., Snyder, J. A., Lockatell, V., Blomfield, I., Johnson, D. E. & Mobley, H. L. ( 2002; ). Assessment of virulence of uropathogenic Escherichia coli type 1 fimbrial mutants in which the invertible element is phase-locked on or off. Infect Immun 70, 3344–3354.[CrossRef]
    [Google Scholar]
  16. Hoffman, J. A., Wass, C., Stins, M. F. & Kim, K. S. ( 1999; ). The capsule supports survival but not traversal of Escherichia coli K1 across the blood–brain barrier. Infect Immun 67, 3566–3570.
    [Google Scholar]
  17. Huang, S. H. & Jong, A. Y. ( 2001; ). Cellular mechanisms of microbial proteins contributing to invasion of the blood–brain barrier. Cell Microbiol 3, 277–287.[CrossRef]
    [Google Scholar]
  18. Huang, S. H., Wass, C., Fu, Q., Prasadarao, N. V., Stins, M. & Kim, K. S. ( 1995; ). Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect Immun 63, 4470–4475.
    [Google Scholar]
  19. Huang, S. H., Chen, Y. H., Kong, G., Chen, S. H., Besemer, J., Borodovsky, M. & Jong, A. ( 2001a; ). A novel genetic island of meningitic Escherichia coli K1 containing the ibeA invasion gene (GimA): functional annotation and carbon-source-regulated invasion of human brain microvascular endothelial cells. Funct Integr Genomics 1, 312–322.[CrossRef]
    [Google Scholar]
  20. Huang, S. H., Wan, Z. S., Chen, Y. H., Jong, A. Y. & Kim, K. S. ( 2001b; ). Further characterization of Escherichia coli brain microvascular endothelial cell invasion gene ibeA by deletion, complementation, and protein expression. J Infect Dis 183, 1071–1078.[CrossRef]
    [Google Scholar]
  21. Johnson, J. R., Swanson, J. L., Barela, T. J. & Brown, J. J. ( 1997; ). Receptor specificities of variant Gal(alpha1-4)Gal-binding PapG adhesins of uropathogenic Escherichia coli as assessed by hemagglutination phenotypes. J Infect Dis 175, 373–381.[CrossRef]
    [Google Scholar]
  22. 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]
  23. Johnson, J. R., Delavari, P. & O'Bryan, T. T. ( 2001b; ). Escherichia coli O18 : K1 : H7 isolates from patients with acute cystitis and neonatal meningitis exhibit common phylogenetic origins and virulence factor profiles. J Infect Dis 183, 425–434.[CrossRef]
    [Google Scholar]
  24. Johnson, J. R., Murray, A. C., Gajewski, A., Sullivan, M., Snippes, P., Kuskowski, M. A. & Smith, K. E. ( 2003; ). Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob Agents Chemother 47, 2161–2168.[CrossRef]
    [Google Scholar]
  25. Kim, K. S. ( 2001; ). Escherichia coli translocation at the blood–brain barrier. Infect Immun 69, 5217–5222.[CrossRef]
    [Google Scholar]
  26. Kim, K. J., Elliott, S. J., Di Cello, F., Stins, M. F. & Kim, K. S. ( 2003; ). The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells. Cell Microbiol 5, 245–252.[CrossRef]
    [Google Scholar]
  27. Lafont, J. P., Dho, M., D'Hauteville, H. M., Bree, A. & Sansonetti, P. J. ( 1987; ). Presence and expression of aerobactin genes in virulent avian strains of Escherichia coli. Infect Immun 55, 193–197.
    [Google Scholar]
  28. La Ragione, R. M. & Woodward, M. J. ( 2002; ). Virulence factors of Escherichia coli serotypes associated with avian colisepticaemia. Res Vet Sci 73, 27–35.[CrossRef]
    [Google Scholar]
  29. La Ragione, R. M., Cooley, W. A. & Woodward, M. J. ( 2000a; ). The role of fimbriae and flagella in the adherence of avian strains of Escherichia coli O78 : K80 to tissue culture cells and tracheal and gut explants. J Med Microbiol 49, 327–338.
    [Google Scholar]
  30. La Ragione, R. M., Sayers, A. R. & Woodward, M. J. ( 2000b; ). The role of fimbriae and flagella in the colonization, invasion and persistence of Escherichia coli O78 : K80 in the day-old-chick model. Epidemiol Infect 124, 351–363.[CrossRef]
    [Google Scholar]
  31. Marc, D., Arne, P., Bree, A. & Dho-Moulin, M. ( 1998; ). Colonization ability and pathogenic properties of a fim mutant of an avian strain of Escherichia coli. Res Microbiol 149, 473–485.[CrossRef]
    [Google Scholar]
  32. Mellata, M., Dho-Moulin, M., Dozois, C. M., Curtiss, R., 3rd, Brown, P. K., Arne, P., Bree, A., Desautels, C. & Fairbrother, J. M. ( 2003a; ). Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect Immun 71, 536–540.[CrossRef]
    [Google Scholar]
  33. Mellata, M., Dho-Moulin, M., Dozois, C. M., Curtiss, R., 3rd, Lehoux, B. & Fairbrother, J. M. ( 2003b; ). Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infect Immun 71, 494–503.[CrossRef]
    [Google Scholar]
  34. Mobley, H. L., Jarvis, K. G., Elwood, J. P., Whittle, D. I., Lockatell, C. V., Russell, R. G., Johnson, D. E., Donnenberg, M. S. & Warren, J. W. ( 1993; ). Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: the role of alpha Gal(1–4) beta Gal binding in virulence of a wild-type strain. Mol Microbiol 10, 143–155.[CrossRef]
    [Google Scholar]
  35. Nakamura, K., Ueda, H., Tanimura, T. & Noguchi, K. ( 1994; ). Effect of mixed live vaccine (Newcastle disease and infectious bronchitis) and Mycoplasma gallisepticum on the chicken respiratory tract and on Escherichia coli infection. J Comp Pathol 111, 33–42.[CrossRef]
    [Google Scholar]
  36. Obata-Yasuoka, M., Ba-Thein, W., Tsukamoto, T., Yoshikawa, H. & Hayashi, H. ( 2002; ). Vaginal Escherichia coli share common virulence factor profiles, serotypes and phylogeny with other extraintestinal E. coli. Microbiology 148, 2745–2752.
    [Google Scholar]
  37. Ochman, H. & Selander, R. K. ( 1984; ). Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157, 690–693.
    [Google Scholar]
  38. Parreira, V. R. & Gyles, C. L. ( 2002; ). Shiga toxin genes in avian Escherichia coli. Vet Microbiol 87, 341–352.[CrossRef]
    [Google Scholar]
  39. Parreira, V. R. & Gyles, C. L. ( 2003; ). A novel pathogenicity island integrated adjacent to the thrW tRNA gene of avian pathogenic Escherichia coli encodes a vacuolating autotransporter toxin. Infect Immun 71, 5087–5096.[CrossRef]
    [Google Scholar]
  40. Picard, B., Garcia, J. S., Gouriou, S., Duriez, P., Brahimi, N., Bingen, E., Elion, J. & Denamur, E. ( 1999; ). The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67, 546–553.
    [Google Scholar]
  41. Pourbakhsh, S. A., Dho-Moulin, M., Bree, A., Desautels, C., Martineau-Doize, B. & Fairbrother, J. M. ( 1997; ). Localization of the in vivo expression of P and F1 fimbriae in chickens experimentally inoculated with pathogenic Escherichia coli. Microb Pathog 22, 331–341.[CrossRef]
    [Google Scholar]
  42. Prasadarao, N. V., Wass, C. A., Weiser, J. N., Stins, M. F., Huang, S. H. & Kim, K. S. ( 1996; ). Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64, 146–153.
    [Google Scholar]
  43. Prasadarao, N. V., Wass, C. A., Huang, S. H. & Kim, K. S. ( 1999; ). Identification and characterization of a novel Ibe10 binding protein that contributes to Escherichia coli invasion of brain microvascular endothelial cells. Infect Immun 67, 1131–1138.
    [Google Scholar]
  44. Provence, D. L. & Curtiss, R., 3rd ( 1994; ). Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect Immun 62, 1369–1380.
    [Google Scholar]
  45. Reingold, J., Starr, N., Maurer, J. & Lee, M. D. ( 1999; ). Identification of a new Escherichia coli She haemolysin homolog in avian E. coli. Vet Microbiol 66, 125–134.[CrossRef]
    [Google Scholar]
  46. Russo, T. A. & Johnson, J. R. ( 2000; ). Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181, 1753–1754.[CrossRef]
    [Google Scholar]
  47. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  48. Stordeur, P., Marlier, D., Blanco, J., Oswald, E., Biet, F., Dho-Moulin, M. & Mainil, J. ( 2002; ). Examination of Escherichia coli from poultry for selected adhesin genes important in disease caused by mammalian pathogenic E. coli. Vet Microbiol 84, 231–241.[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. Vandemaele, F. J., Mugasa, J. P., Vandekerchove, D. & Goddeeris, B. M. ( 2003; ). Predominance of the papGII allele with high sequence homology to that of human isolates among avian pathogenic Escherichia coli (APEC). Vet Microbiol 97, 245–257.[CrossRef]
    [Google Scholar]
  51. Wang, Y., Huang, S. H., Wass, C. A., Stins, M. F. & Kim, K. S. ( 1999; ). The gene locus yijP contributes to Escherichia coli K1 invasion of brain microvascular endothelial cells. Infect Immun 67, 4751–4756.
    [Google Scholar]
  52. Weiser, J. N. & Gotschlich, E. C. ( 1991; ). Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun 59, 2252–2258.
    [Google Scholar]
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