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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28677-0
2006-04-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/4/1143.html?itemId=/content/journal/micro/10.1099/mic.0.28677-0&mimeType=html&fmt=ahah

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 Microbiol 48, 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 Bacteriol 152, 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 Microbiol 148, 745–755.[CrossRef]
    [Google Scholar]
  4. Blomfield, I. C. ( 2001; ). The regulation of pap and type 1 fimbriation in Escherichia coli. Adv Microbiol Physiol 45, 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 Microbiol 5, 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 Microbiol 5, 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 Bacteriol 175, 27–36.
    [Google Scholar]
  8. Brody, J. R. & Kern, S. E. ( 2004; ). Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques 36, 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 A 97, 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 III536 of uropathogenic Escherichia coli strain 536. Infect Immun 69, 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 Microbiol 49, 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 Immun 18, 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 Microbiol 12, 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 Microbiol 40, 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 Bacteriol 175, 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 Bacteriol 176, 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 Microbiol 21, 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 Pathol 54, 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 Immun 69, 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 Immun 69, 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 Biology, vol. 45, pp. 135–140. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  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 Microbiol 33, 693–703.[CrossRef]
    [Google Scholar]
  23. Holden, N. J. & Gally, D. L. ( 2004; ). Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol 53, 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 Microbiol 42, 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 Immun 33, 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 Pathog 17, 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 Microbiol 36, 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 Immun 67, 429–432.
    [Google Scholar]
  29. Johnson, J. R. ( 1991; ). Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4, 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 Urol 169, 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 J 5, 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 Bacteriol 168, 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 Microbiol 28, 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 Immun 66, 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 J 3, 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 Microbiol 6, 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 Bacteriol 173, 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. Nephron 77, 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 Immun 58, 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 Microbiol 10, 143–155.[CrossRef]
    [Google Scholar]
  41. Naber, K. G. ( 2000; ). Survey on antibiotic usage in the treatment of urinary tract infections. J Antimicrob Chemother 46 (Supplement 1), 49–52.[CrossRef]
    [Google Scholar]
  42. Nicolle, L. E. ( 2001; ). Epidemiology of urinary tract infection. Infect Med 18, 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 J 3, 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 J 14, 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 Bacteriol 160, 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 Dis 156, 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 Microbiol 54, 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 Bacteriol 183, 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 Immun 71, 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 Microbiol 54, 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 Microbiol 49, 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.
  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 Immun 71, 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 Immun 70, 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 Immun 73, 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 Immun 73, 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 J 19, 1450–1457.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28677-0
Loading
/content/journal/micro/10.1099/mic.0.28677-0
Loading

Data & Media loading...

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