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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066472-0
2013-08-01
2020-07-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/8/1606.html?itemId=/content/journal/micro/10.1099/mic.0.066472-0&mimeType=html&fmt=ahah

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 A82:5724–5727 [CrossRef][PubMed]
    [Google Scholar]
  2. Altman D. G., Bland J. M..( 1994;). Diagnostic tests. 1: Sensitivity and specificity. BMJ308:1552 [CrossRef][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 Res25:3389–3402 [CrossRef][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 Microbiol48:3455–3456 [CrossRef][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 Microbiol83:908–925 [CrossRef]
    [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 Bacteriol152:1241–1247[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. Science277:1453–1462 [CrossRef][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 Lett126:189–195[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 Bacteriol180:1159–1165[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 Immun74:1072–1083 [CrossRef][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 Microbiol10:161 [CrossRef][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 A103:5977–5982 [CrossRef][PubMed]
    [Google Scholar]
  13. Clermont O., Bonacorsi S., Bingen E..( 2000;). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol66:4555–4558 [CrossRef][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 A93:9827–9832 [CrossRef][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 Microbiol74:1071–1082 [CrossRef][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 Dis200:528–536 [CrossRef][PubMed]
    [Google Scholar]
  17. Dobrindt U., Hochhut B., Hentschel U., Hacker J..( 2004;). Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol2:414–424 [CrossRef][PubMed]
    [Google Scholar]
  18. Foxman B..( 2010;). The epidemiology of urinary tract infection. Nat Rev Urol7:653–660 [CrossRef][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 Epidemiol10:509–515 [CrossRef][PubMed]
    [Google Scholar]
  20. Gal-Mor O., Finlay B. B..( 2006;). Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol8:1707–1719 [CrossRef][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 Microbiol21:725–738 [CrossRef][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 Immun75:52–60 [CrossRef][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 Microbiol10:2484–2496 [CrossRef][PubMed]
    [Google Scholar]
  24. Groisman E. A., Ochman H..( 1994;). How to become a pathogen. Trends Microbiol2:289–294 [CrossRef][PubMed]
    [Google Scholar]
  25. Hacker J..( 1990;). Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli. Curr Top Microbiol Immunol151:1–27 [CrossRef][PubMed]
    [Google Scholar]
  26. Hacker J., Kaper J. B..( 2000;). Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol54:641–679 [CrossRef][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 Ser41:95–98
    [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 Microbiol67:116–128[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 Bacteriol172:6175–6181[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 Med335:468–474 [CrossRef][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 Immun63:4470–4475[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 Immun33:933–938[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 Immun54:613–620[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 Dis181:261–272 [CrossRef][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 Dis156:225–229 [CrossRef][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 Immun56:405–412[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 Dis163:325–330 [CrossRef][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 Dis183:78–88 [CrossRef][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 Bacteriol188:5356–5363 [CrossRef][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 Res33:Database issueD297–D302 [CrossRef][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 J5:1389–1393[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 Care17:50–57 [CrossRef][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 Microbiol30:1189–1193[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 Evol15:1685–1695 [CrossRef][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 Bacteriol189:3532–3546 [CrossRef][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 Bacteriol173:5308–5314[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 Immun58:1281–1289[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. Science282:1494–1497 [CrossRef][PubMed]
    [Google Scholar]
  49. Ochman H., Selander R. K..( 1984;). Standard reference strains of Escherichia coli from natural populations. J Bacteriol157:690–693[PubMed]
    [Google Scholar]
  50. Ørskov F., Ørskov I..( 1992;). Escherichia coli serotyping and disease in man and animals. Can J Microbiol38:699–704 [CrossRef][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 Stand92:117–122[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 Immun67:546–553[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 Med308:681–685 [CrossRef][PubMed]
    [Google Scholar]
  54. Rushton H. G..( 1997;). Urinary tract infections in children. Epidemiology, evaluation, and management. Pediatr Clin North Am44:1133–1169 [CrossRef][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 Infect5:449–456 [CrossRef][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 Dis163:773–779 [CrossRef][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 Sci7:75–89[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 Res22:4673–4680 [CrossRef][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 Dis150:728–736 [CrossRef][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 Microbiol9:2230–2241 [CrossRef][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 Immun74:4039–4047 [CrossRef][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 Microbiol12:85–90 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066472-0
Loading
/content/journal/micro/10.1099/mic.0.066472-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error