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
2020-04-02
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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 Immun51:268–276
    [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 Microbiol45:1079–1093[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. Nature279:778–781[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 Microbiol35:2953–2957
    [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 Microbiol61:229–235[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 Microbiol32:1197–1202
    [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 Microbiol94:97–103[CrossRef]
    [Google Scholar]
  9. Dho-Moulin M., Fairbrother J. M. 1999; Avian pathogenic Escherichia coli (APEC). Vet Res30:299–316
    [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 Dis26:787–797[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 Immun59:4310–4317
    [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 Immun60:2648–2656
    [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. Microbiology142:2759–2766[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 Immun68:4145–4154[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 Immun70:3344–3354[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 Immun67:3566–3570
    [Google Scholar]
  17. Huang S. H., Jong A. Y. 2001; Cellular mechanisms of microbial proteins contributing to invasion of the blood–brain barrier. Cell Microbiol3:277–287[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 Immun63:4470–4475
    [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 Genomics1:312–322[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 Dis183:1071–1078[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 Dis175:373–381[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 Dis183:78–88[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 Dis183:425–434[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 Chemother47:2161–2168[CrossRef]
    [Google Scholar]
  25. Kim K. S. 2001; Escherichia coli translocation at the blood–brain barrier. Infect Immun69:5217–5222[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 Microbiol5:245–252[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 Immun55:193–197
    [Google Scholar]
  28. La Ragione R. M., Woodward M. J. 2002; Virulence factors of Escherichia coli serotypes associated with avian colisepticaemia. Res Vet Sci73:27–35[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 Microbiol49:327–338
    [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 Infect124:351–363[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 Microbiol149:473–485[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 Immun71:536–540[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 Immun71:494–503[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 Microbiol10:143–155[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 Pathol111:33–42[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 extraintestinalE. coli. Microbiology148:2745–2752
    [Google Scholar]
  37. Ochman H., Selander R. K. 1984; Standard reference strains of Escherichia coli from natural populations. J Bacteriol157:690–693
    [Google Scholar]
  38. Parreira V. R., Gyles C. L. 2002; Shiga toxin genes in avian Escherichia coli. Vet Microbiol87:341–352[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 Immun71:5087–5096[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 Immun67:546–553
    [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 Pathog22:331–341[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 Immun64:146–153
    [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 Immun67:1131–1138
    [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 Immun62:1369–1380
    [Google Scholar]
  45. Reingold J., Starr N., Maurer J., Lee M. D. 1999; Identification of a new Escherichia coli She haemolysin homolog in avianE. coli. Vet Microbiol66:125–134[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 Dis181:1753–1754[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;
    [Google Scholar]
  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 pathogenicE. coli. Vet Microbiol84:231–241[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 Immun69:6179–6185[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 Microbiol97:245–257[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 Immun67:4751–4756
    [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 Immun59:2252–2258
    [Google Scholar]
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