1887

Abstract

Uropathogenic (UPEC) fall within a larger group of isolates producing extraintestinal disease. UPEC express type 1 pili as a critical virulence determinant mediating adherence to and invasion into urinary tract tissues. Type 1 pili expression is under regulation by a family of site-specific recombinases, including FimX, which is encoded from a genomic island called PAI-X for thogenicity sland of Fim. Using a new multiplex PCR, and the additional PAI-X genes were found to be highly associated with UPEC (144/173 = 83.2 %), and more prevalent in UPEC of lower urinary tract origin (105/120 = 87.5 %) than upper urinary tract origin (39/53 = 74 %; <0.05) or commensal isolates (28/78 = 36 %; ≤0.0001). The Fim-like recombinase gene is the only family member that has a significant association with UPEC compared to commensal isolates. Our results indicate PAI-X genes, including the type 1 pili regulator gene , are highly prevalent among UPEC isolates and have a strong positive correlation with genomic virulence factors, suggesting a potential role for PAI-X in the extraintestinal pathogenic lifestyle.

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2013-08-01
2022-01-18
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References

  1. Abraham J. M., Freitag C. S., Clements J. R., Eisenstein B. I.( 1985). An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A 82:5724–5727 [View Article][PubMed]
    [Google Scholar]
  2. Altman D. G., Bland J. M.( 1994). Diagnostic tests. 1: Sensitivity and specificity. BMJ 308:1552 [View Article][PubMed]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.( 1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  4. Bailey J. K., Pinyon J. L., Anantham S., Hall R. M.( 2010). Distribution of human commensal Escherichia coli phylogenetic groups. J Clin Microbiol 48:3455–3456 [View Article][PubMed]
    [Google Scholar]
  5. Bateman S. L., Seed P. C.( 2012). Epigenetic regulation of the nitrosative stress response and intracellular macrophage survival by extraintestinal pathogenic. Escherichia coli. Mol Microbiol 83:908–925 [View Article]
    [Google Scholar]
  6. Berger H., Hacker J., Juarez A., Hughes C., Goebel W.( 1982). Cloning of the chromosomal determinants encoding hemolysin production and mannose-resistant hemagglutination in Escherichia coli. J Bacteriol 152:1241–1247[PubMed]
    [Google Scholar]
  7. Blattner F. R., Plunkett G. III, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K.& other authors ( 1997). The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462 [View Article][PubMed]
    [Google Scholar]
  8. Blum G., Falbo V., Caprioli A., Hacker J.( 1995). Gene clusters encoding the cytotoxic necrotizing factor type 1, Prs-fimbriae and alpha-hemolysin form the pathogenicity island II of the uropathogenic Escherichia coli strain J96. FEMS Microbiol Lett 126:189–195[PubMed]
    [Google Scholar]
  9. Boyd E. F., Hartl D. L.( 1998). Chromosomal regions specific to pathogenic isolates of Escherichia coli have a phylogenetically clustered distribution. J Bacteriol 180:1159–1165[PubMed]
    [Google Scholar]
  10. Bryan A., Roesch P., Davis L., Moritz R., Pellett S., Welch R. A.( 2006). Regulation of type 1 fimbriae by unlinked FimB- and FimE-like recombinases in uropathogenic Escherichia coli strain CFT073. Infect Immun 74:1072–1083 [View Article][PubMed]
    [Google Scholar]
  11. Carlos C., Pires M. M., Stoppe N. C., Hachich E. M., Sato M. I., Gomes T. A., Amaral L. A., Ottoboni L. M.( 2010). Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol 10:161 [View Article][PubMed]
    [Google Scholar]
  12. 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 [View Article][PubMed]
    [Google Scholar]
  13. Clermont O., Bonacorsi S., Bingen E.( 2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558 [View Article][PubMed]
    [Google Scholar]
  14. Connell I., Agace W., Klemm P., Schembri M., Mărild S., Svanborg C.( 1996). Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A 93:9827–9832 [View Article][PubMed]
    [Google Scholar]
  15. Corcoran C. P., Dorman C. J.( 2009). DNA relaxation-dependent phase biasing of the fim genetic switch in Escherichia coli depends on the interplay of H-NS, IHF and LRP. Mol Microbiol 74:1071–1082 [View Article][PubMed]
    [Google Scholar]
  16. Czaja C. A., Stamm W. E., Stapleton A. E., Roberts P. L., Hawn T. R., Scholes D., Samadpour M., Hultgren S. J., Hooton T. M.( 2009). Prospective cohort study of microbial and inflammatory events immediately preceding Escherichia coli recurrent urinary tract infection in women. J Infect Dis 200:528–536 [View Article][PubMed]
    [Google Scholar]
  17. Dobrindt U., Hochhut B., Hentschel U., Hacker J.( 2004). Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424 [View Article][PubMed]
    [Google Scholar]
  18. Foxman B.( 2010). The epidemiology of urinary tract infection. Nat Rev Urol 7:653–660 [View Article][PubMed]
    [Google Scholar]
  19. 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 [View Article][PubMed]
    [Google Scholar]
  20. Gal-Mor O., Finlay B. B.( 2006). Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8:1707–1719 [View Article][PubMed]
    [Google Scholar]
  21. Gally D. L., Leathart J., Blomfield I. C.( 1996). Interaction of FimB and FimE with the fim switch that controls the phase variation of type 1 fimbriae in Escherichia coli K-12. Mol Microbiol 21:725–738 [View Article][PubMed]
    [Google Scholar]
  22. Garofalo C. K., Hooton T. M., Martin S. M., Stamm W. E., Palermo J. J., Gordon J. I., Hultgren S. J.( 2007). Escherichia coli from urine of female patients with urinary tract infections is competent for intracellular bacterial community formation. Infect Immun 75:52–60 [View Article][PubMed]
    [Google Scholar]
  23. Gordon D. M., Clermont O., Tolley H., Denamur E.( 2008). Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 10:2484–2496 [View Article][PubMed]
    [Google Scholar]
  24. Groisman E. A., Ochman H.( 1994). How to become a pathogen. Trends Microbiol 2:289–294 [View Article][PubMed]
    [Google Scholar]
  25. Hacker J.( 1990). Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli. Curr Top Microbiol Immunol 151:1–27 [View Article][PubMed]
    [Google Scholar]
  26. Hacker J., Kaper J. B.( 2000). Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54:641–679 [View Article][PubMed]
    [Google Scholar]
  27. Hall T. A.( 1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  28. Hannan T. J., Mysorekar I. U., Chen S. L., Walker J. N., Jones J. M., Pinkner J. S., Hultgren S. J., Seed P. C.( 2008). LeuX tRNA-dependent and -independent mechanisms of Escherichia coli pathogenesis in acute cystitis. Mol Microbiol 67:116–128[PubMed]
    [Google Scholar]
  29. Herzer P. J., Inouye S., Inouye M., Whittam T. S.( 1990). Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181[PubMed]
    [Google Scholar]
  30. Hooton T. M., Scholes D., Hughes J. P., Winter C., Roberts P. L., Stapleton A. E., Stergachis A., Stamm W. E.( 1996). A prospective study of risk factors for symptomatic urinary tract infection in young women. N Engl J Med 335:468–474 [View Article][PubMed]
    [Google Scholar]
  31. 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[PubMed]
    [Google Scholar]
  32. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S.( 1981). Construction and expression of recombinant plasmids encoding type 1 or d-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun 33:933–938[PubMed]
    [Google Scholar]
  33. Hultgren S. J., Schwan W. R., Schaeffer A. J., Duncan J. L.( 1986). Regulation of production of type 1 pili among urinary tract isolates of Escherichia coli. Infect Immun 54:613–620[PubMed]
    [Google Scholar]
  34. 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 [View Article][PubMed]
    [Google Scholar]
  35. Johnson J. R., Roberts P. L., Stamm W. E.( 1987). P fimbriae and other virulence factors in Escherichia coli urosepsis: association with patients’ characteristics. J Infect Dis 156:225–229 [View Article][PubMed]
    [Google Scholar]
  36. Johnson J. R., Moseley S. L., Roberts P. L., Stamm W. E.( 1988). Aerobactin and other virulence factor genes among strains of Escherichia coli causing urosepsis: association with patient characteristics. Infect Immun 56:405–412[PubMed]
    [Google Scholar]
  37. Johnson J. R., Lyons M. F. II, Pearce W., Gorman P., Roberts P. L., White N., Brust P., Olsen R., Gnann J. W. Jr, Stamm W. E.( 1991). Therapy for women hospitalized with acute pyelonephritis: a randomized trial of ampicillin versus trimethoprim-sulfamethoxazole for 14 days. J Infect Dis 163:325–330 [View Article][PubMed]
    [Google Scholar]
  38. Johnson J. R., Delavari P., Kuskowski M., Stell A. L.( 2001). Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183:78–88 [View Article][PubMed]
    [Google Scholar]
  39. Kelly A., Conway C., O Cróinín T., Smith S. G., Dorman C. J.( 2006). DNA supercoiling and the Lrp protein determine the directionality of fim switch DNA inversion in Escherichia coli K-12. J Bacteriol 188:5356–5363 [View Article][PubMed]
    [Google Scholar]
  40. Kersey P., Bower L., Morris L., Horne A., Petryszak R., Kanz C., Kanapin A., Das U., Michoud K.& other authors ( 2005). Integr8 and genome reviews: integrated views of complete genomes and proteomes. Nucleic Acids Res 33:Database issueD297–D302 [View Article][PubMed]
    [Google Scholar]
  41. Klemm P.( 1986). Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J 5:1389–1393[PubMed]
    [Google Scholar]
  42. Laupland K. B., Zygun D. A., Davies H. D., Church D. L., Louie T. J., Doig C. J.( 2002). Incidence and risk factors for acquiring nosocomial urinary tract infection in the critically ill. J Crit Care 17:50–57 [View Article][PubMed]
    [Google Scholar]
  43. Le Bouguenec C., Archambaud M., Labigne A.( 1992). Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J Clin Microbiol 30:1189–1193[PubMed]
    [Google Scholar]
  44. Lecointre G., Rachdi L., Darlu P., Denamur E.( 1998). Escherichia coli molecular phylogeny using the incongruence length difference test. Mol Biol Evol 15:1685–1695 [View Article][PubMed]
    [Google Scholar]
  45. 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 [View Article][PubMed]
    [Google Scholar]
  46. McClain M. S., Blomfield I. C., Eisenstein B. I.( 1991). Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli. J Bacteriol 173:5308–5314[PubMed]
    [Google Scholar]
  47. Mobley H. L., Green D. M., Trifillis A. L., Johnson D. E., Chippendale G. R., Lockatell C. V., Jones B. D., Warren J. W.( 1990). Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58:1281–1289[PubMed]
    [Google Scholar]
  48. 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 [View Article][PubMed]
    [Google Scholar]
  49. Ochman H., Selander R. K.( 1984). Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690–693[PubMed]
    [Google Scholar]
  50. Ørskov F., Ørskov I.( 1992). Escherichia coli serotyping and disease in man and animals. Can J Microbiol 38:699–704 [View Article][PubMed]
    [Google Scholar]
  51. Palaszynski S., Pinkner J., Leath S., Barren P., Auguste C. G., Burlein J., Hultgren S., Langermann S.( 1998). Systemic immunization with conserved pilus-associated adhesins protects against mucosal infections. Dev Biol Stand 92:117–122[PubMed]
    [Google Scholar]
  52. 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[PubMed]
    [Google Scholar]
  53. Riley L. W., Remis R. S., Helgerson S. D., McGee H. B., Wells J. G., Davis B. R., Hebert R. J., Olcott E. S., Johnson L. M.& other authors ( 1983). Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681–685 [View Article][PubMed]
    [Google Scholar]
  54. Rushton H. G.( 1997). Urinary tract infections in children. Epidemiology, evaluation, and management. Pediatr Clin North Am 44:1133–1169 [View Article][PubMed]
    [Google Scholar]
  55. Russo T. A., Johnson J. R.( 2003). Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5:449–456 [View Article][PubMed]
    [Google Scholar]
  56. Stapleton A., Moseley S., Stamm W. E.( 1991). Urovirulence determinants in Escherichia coli isolates causing first-episode and recurrent cystitis in women. J Infect Dis 163:773–779 [View Article][PubMed]
    [Google Scholar]
  57. Svanborg Edén C., Hull R., Falkow S., Leffler H.( 1983). Target cell specificity of wild-type E. coli and mutants and clones with genetically defined adhesins. Prog Food Nutr Sci 7:75–89[PubMed]
    [Google Scholar]
  58. Thompson J. D., Higgins D. G., Gibson T. J.( 1994). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  59. Tullus K., Hörlin K., Svenson S. B., Källenius G.( 1984). Epidemic outbreaks of acute pyelonephritis caused by nosocomial spread of P fimbriated Escherichia coli in children. J Infect Dis 150:728–736 [View Article][PubMed]
    [Google Scholar]
  60. Wright K. J., Seed P. C., Hultgren S. J.( 2007). Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9:2230–2241 [View Article][PubMed]
    [Google Scholar]
  61. Xie Y., Yao Y., Kolisnychenko V., Teng C. H., Kim K. S.( 2006). HbiF regulates type 1 fimbriation independently of FimB and FimE. Infect Immun 74:4039–4047 [View Article][PubMed]
    [Google Scholar]
  62. Yamamoto S., Terai A., Yuri K., Kurazono H., Takeda Y., Yoshida O.( 1995). Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol Med Microbiol 12:85–90 [View Article][PubMed]
    [Google Scholar]
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