1887

Abstract

The majority of strains isolated from urinary tract infections have the potential to express multiple fimbriae. Two of the most common fimbrial adhesins are type 1 fimbriae and pyelonephritis-associated pili (Pap). Previous research has shown that induced, plasmid-based expression of a Pap regulator, , and its close homologues can prevent inversion of the switch controlling the expression of type 1 fimbriae. The aim of the present study was to determine if this cross-regulation occurs when PapB is expressed from its native promoter in the chromosome of K-12 and clinical isolates. The regulation was examined in three ways: (1) mutated alleles of the regulatory region, including and , that maintain the promoter in either the off or the on phase were exchanged into the chromosome of both K-12 and the clinical isolate CFT073, and the effect on type 1 fimbrial expression was measured; (2) type 1 fimbrial expression was determined using a novel  : :  reporter system in mutants of the clinical isolate 536 in which combinations of complete fimbrial clusters had been deleted; (3) type 1 fimbrial expression was determined in a range of clinical isolates and compared with both the number of P clusters and their expression. All three approaches demonstrated that P expression represses type 1 fimbrial expression. Using a number of novel genetic approaches, this work extends the initial finding that PapB inhibits FimB recombination to the impact of this regulation in clinical isolates.

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2006-04-01
2020-08-03
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References

  1. Barnich N, Boudeau J, Claret L, Darfeuille-Michaud A. 2003; Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease. Mol Microbiol48:781–794[CrossRef]
    [Google Scholar]
  2. Berger H, Hacker J, Juarez A, Hughes C, Goebel W. 1982; Cloning of the chromosomal determinants encoding haemolysin production and mannose-resistant haemagglutination in Escherichia coli . J Bacteriol152:1241–1247
    [Google Scholar]
  3. Blanco M, Blanco J. E, Alonso M. P, Mora A, Balsalobre C, Munoa F, Juarez A, Blanco J. 1997; Detection of pap , sfa and afa adhesin-encoding operons in uropathogenic Escherichia coli strains: relationship with expression of adhesins and production of toxins. Res Microbiol148:745–755[CrossRef]
    [Google Scholar]
  4. Blomfield I. C. 2001; The regulation of pap and type 1 fimbriation in Escherichia coli . Adv Microbiol Physiol45:1–49
    [Google Scholar]
  5. Blomfield I. C, Mcclain M. S, Eisenstein B. I. 1991; Type 1 fimbriae mutants of Escherichia coli K12 – characterization of recognized afimbriate strains and construction of new fim deletion mutants. Mol Microbiol5:1439–1445[CrossRef]
    [Google Scholar]
  6. Blomfield I. C, Vaughn V, Rest R. F, Eisenstein B. I. 1991; Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol5:1447–1457[CrossRef]
    [Google Scholar]
  7. Blomfield I. C, Calie P. J, Eberhardt K. J, Mcclain M. S, Eisenstein B. I. 1993; Lrp stimulates phase variation of type 1 fimbriation in Escherichia coli K12. J Bacteriol175:27–36
    [Google Scholar]
  8. Brody J. R, Kern S. E. 2004; Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques36:214–216
    [Google Scholar]
  9. Datsenko K. A, Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645[CrossRef]
    [Google Scholar]
  10. 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[sub]536[/sub] of uropathogenic Escherichia coli strain 536. Infect Immun69:4248–4256[CrossRef]
    [Google Scholar]
  11. El-Labany S, Sohanpal B. K, Lahooti M, Akerman R, Blomfield I. C. 2003; Distant cis -active sequences and sialic acid control the expression of fimB in Escherichia coli K-12. Mol Microbiol49:1109–1118[CrossRef]
    [Google Scholar]
  12. Evans D. G, Evans D. J., Jr, Tjoa W. 1977; Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun18:330–337
    [Google Scholar]
  13. Evans D. J., Jr, Evans D. G, Young L. S, Pitt J. 1980; Hemagglutination typing of Escherichia coli : definition of seven hemagglutination types. J Clin Microbiol12:235–242
    [Google Scholar]
  14. Frendeus B, Wachtler C, Hedlund M, Fischer H, Samuelsson P, Svensson M, Svanborg C. 2001; Escherichia coli P fimbriae utilize the Toll-like receptor 4 pathway for cell activation. Mol Microbiol40:37–51[CrossRef]
    [Google Scholar]
  15. Gally D. L, Bogan J. A, Eisenstein B. I, Blomfield I. C. 1993; Environmental-regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12 – effects of temperature and media. J Bacteriol175:6186–6193
    [Google Scholar]
  16. Gally D. L, Rucker T. J, Blomfield I. C. 1994; The leucine-responsive regulatory protein binds to the fim switch to control phase variation of type 1 fimbrial expression in Escherichia coli K12. J Bacteriol176:5665–5672
    [Google Scholar]
  17. 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]
    [Google Scholar]
  18. Graham J. C, Galloway A. 2001; ACP Best Practice No 167: the laboratory diagnosis of urinary tract infection. J Clin Pathol54:911–919[CrossRef]
    [Google Scholar]
  19. Graham J. C, Leathart J. B. S, Keegan S. J, Pearson J, Bint A, Gally D. L. 2001; Analysis of Escherichia coli strains causing bacteriuria during pregnancy: selection for strains that do not express type 1 fimbriae. Infect Immun69:794–799[CrossRef]
    [Google Scholar]
  20. Gunther N. W, Lockatell V, Johnson D. E, Mobley H. L. T. 2001; In vivo dynamics of type 1 fimbria regulation in uropathogenic Escherichia coli during experimental urinary tract infection. Infect Immun69:2838–2846[CrossRef]
    [Google Scholar]
  21. Guyer M. S, Reed R. R, Steitz J. A, Low K. B. 1981; Identification of a sex-factor-affinity site in Escherichia coli as a gamma delta.. In Cold Spring Harbor Symposium on Quantitiative Biologyvol. 45 pp 135–140 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Hedlund M, Wachtler C, Johansson E, Hang L, Somerville J. E, Darveau R. P, Svanborg C. 1999; P fimbriae-dependent, lipopolysaccharide-independent activation of epithelial cytokine responses. Mol Microbiol33:693–703[CrossRef]
    [Google Scholar]
  23. Holden N. J, Gally D. L. 2004; Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol53:585–593[CrossRef]
    [Google Scholar]
  24. Holden N. J, Uhlin B. E, Gally D. L. 2001; PapB paralogues and their effect on the phase variation of type 1 fimbriae in Escherichia coli . Mol Microbiol42:319–330[CrossRef]
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Hull R. A, Nowicki B, Kaul A, Runyan R, Svanborg C, Hull S. I. 1994; Effect of Pap copy number and receptor specificity on virulence of fimbriated Escherichia coli in a murine urinary-tract colonization model. Microb Pathog17:79–86[CrossRef]
    [Google Scholar]
  27. Hull R. A, Rudy D. C, Wieser I. E, Donovan W. H. 1998; Virulence factors of Escherichia coli isolates from patients with symptomatic and asymptomatic bacteriuria and neuropathic bladders due to spinal cord and brain injuries. J Clin Microbiol36:115–117
    [Google Scholar]
  28. Hull R. A, Rudy D. C, Donovan W. H, Wieser I. E, Stewart C, Darouiche R. O. 1999; Virulence properties of Escherichia coli 83972, a prototype strain associated with asymptomatic bacteriuria. Infect Immun67:429–432
    [Google Scholar]
  29. Johnson J. R. 1991; Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev4:80–128
    [Google Scholar]
  30. Keegan S. J, Graham C, Neal D. E, Blum-Oehler G, N'Dow J, Pearson J. P, Gally D. L. 2003; Characterization of Escherichia coli strains causing urinary tract infections in patients with transposed intestinal segments. J Urol169:2382–2387[CrossRef]
    [Google Scholar]
  31. Klemm P. 1986; 2 regulatory fim genes, fimB and fimE , control the phase variation of type 1 fimbriae in Escherichia coli . EMBO J5:1389–1393
    [Google Scholar]
  32. Knapp S, Hacker J, Jarchau T, Goebel W. 1986; Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol168:22–30
    [Google Scholar]
  33. Leathart J. B. S, Gally D. L. 1998; Regulation of type 1 fimbrial expression in uropathogenic Escherichia coli : heterogeneity of expression through sequence changes in the fim switch region. Mol Microbiol28:371–381[CrossRef]
    [Google Scholar]
  34. Lim J. K, Gunther N. W, Zhao H, Johnson D. E, Keay S. K, Mobley H. L. T. 1998; In vivo phase variation of Escherichia coli type 1 fimbrial genes in women with urinary tract infection. Infect Immun66:3303–3310
    [Google Scholar]
  35. Lindberg F. P, Lund B, Normark S. 1984; Genes of pyelonephritogenic Escherichia coli required for digalactoside-specific agglutination of human cells. EMBO J3:1167–1173
    [Google Scholar]
  36. Marklund B. I, Tennent J. M, Garcia E, Hamers A, Baga M, Lindberg F, Gaastra W, Normark S. 1992; Horizontal gene transfer of the Escherichia coli Pap and Prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol6:2225–2242[CrossRef]
    [Google Scholar]
  37. 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
    [Google Scholar]
  38. Mizunoe Y, Matsumoto T, Sakumoto M, Kubo S, Mochida O, Sakamoto Y, Kumazawa J. 1997; Renal scarring by mannose-sensitive adhesin of Escherichia coli type 1 pili. Nephron77:412–416[CrossRef]
    [Google Scholar]
  39. 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
    [Google Scholar]
  40. Mobley H, 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]
  41. Naber K. G. 2000; Survey on antibiotic usage in the treatment of urinary tract infections. J Antimicrob Chemother46:Supplement 149–52[CrossRef]
    [Google Scholar]
  42. Nicolle L. E. 2001; Epidemiology of urinary tract infection. Infect Med18:153–162
    [Google Scholar]
  43. Norgren M, Normark S, Lark D, O'Hanley P, Schoolnik G, Falkow S, Svanborg-Eden C, Baga M, Uhlin B. E. 1984; Mutations in Eschericha coli cistrons affecting adhesion to human cells do not abolish Pap pili fiber formation. EMBO J3:1159–1165
    [Google Scholar]
  44. Nou X. W, Braaten B, Kaltenbach L, Low D. A. 1995; Differential binding of Lrp to 2 sets of pap DNA-binding sites mediated by papI regulates pap phase variation in Escherichia coli . EMBO J14:5785–5797
    [Google Scholar]
  45. Nowicki B, Rhen M, Vaisanenrhen V, Pere A, Korhonen T. K. 1984; Immunofluorescence study of fimbrial phase variation in Escherichia coli KS71. J Bacteriol160:691–695
    [Google Scholar]
  46. Pere A, Nowicki B, Saxen H, Siitonen A, Korhonen T. K. 1987; Escherichia coli in the urine of patients with acute urinary tract infection. J Infect Dis156:567–574[CrossRef]
    [Google Scholar]
  47. Porter M. E, Mitchell P, Roe A. J, Free A, Smith D. G, Gally D. L. 2004; Direct and indirect transcriptional activation of virulence genes by an AraC-like protein, PerA from enteropathogenic Escherichia coli . Mol Microbiol54:1117–1133[CrossRef]
    [Google Scholar]
  48. Pouttu R, Westerlund-Wikstrom B, Lang H, Alsti K, Virkola R, Saarela U, Siitonen A, Kalkkinen N, Korhonen T. K. 2001; matB , a common fimbrillin gene of Escherichia coli , expressed in a genetically conserved, virulent clonal group. J Bacteriol183:4727–4736[CrossRef]
    [Google Scholar]
  49. Roe A. J, Yull H, Naylor S. W, Woodward M. J, Smith D. G. E, Gally D. L. 2003; Heterogeneous surface expression of EspA translocon filaments by Escherichia coli O157 : H7 is controlled at the posttranscriptional level. Infect Immun71:5900–5909[CrossRef]
    [Google Scholar]
  50. Roe A. J, Naylor S. W, Spears K. J.8 other authors 2004; Co-ordinate single-cell expression of LEE4 - and LEE5 -encoded proteins of Escherichia coli O157 : H7. Mol Microbiol54:337–352[CrossRef]
    [Google Scholar]
  51. Roesch P. L, Redford P, Batchelet S, Moritz R. L, Pellett S, Haugen B. J, Blattner F. R, Welch R. A. 2003; Uropathogenic Escherichia coli use d-serine deaminase to modulate infection of the murine urinary tract. Mol Microbiol49:55–67[CrossRef]
    [Google Scholar]
  52. 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]
  53. Schilling J. D, Martin S. M, Hunstad D. A, Patel K. P, Mulvey M. A, Justice S. S, Lorenz R. G, Hultgren S. J. 2003; CD14-and toll-like receptor-dependent activation of bladder epithelial cells by lipopolysaccharide and type 1 piliated Escherichia coli . Infect Immun71:1470–1480[CrossRef]
    [Google Scholar]
  54. Schwan W. R, Lee J. L, Lenard F. A, Matthews B. T, Beck M. T. 2002; Osmolarity and pH growth conditions regulate fim gene transcription and type 1 pilus expression in uropathogenic Escherichia coli . Infect Immun70:1391–1402[CrossRef]
    [Google Scholar]
  55. Schwan W. R, Beck M. T, Hultgren S. J, Pinkner J, Woolever N. L, Larson T. 2005; Down-regulation of the kps region 1 capsular assembly operon following attachment of Escherichia coli Type 1 fimbriae to d-mannose receptors. Infect Immun73:1226–1231[CrossRef]
    [Google Scholar]
  56. 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 Immun73:7588–7596[CrossRef]
    [Google Scholar]
  57. Xia Y, Gally D, Forsman-Semb K, Uhlin B. E. 2000; Regulatory cross-talk between adhesin operons in Escherichia coli : inhibition of type 1 fimbriae expression by the PapB protein. EMBO J19:1450–1457[CrossRef]
    [Google Scholar]
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