Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1989 Nov;57(11):3594–3600. doi: 10.1128/iai.57.11.3594-3600.1989

Purified P fimbriae from two cloned gene clusters of a single pyelonephritogenic strain adhere to unique structures in the human kidney.

J F Karr 1, B Nowicki 1, L D Truong 1, R A Hull 1, S I Hull 1
PMCID: PMC259873  PMID: 2572557

Abstract

We have completed immunofluorescence binding studies of purified fimbriae from two clones which express Pap or Pap-2 fimbriae. Although the two fimbrial types exhibited common binding to the uroepithelia of the bladder and renal pelvis and to occasional cells located within the glomeruli which we have termed glomerular elements, only Pap-2 fimbriae adhered to Bowman's capsule. Previous studies have demonstrated that the Gal alpha 1----4Gal disaccharide moiety is capable of inhibiting Pap hemagglutination and adherence to uroepithelial cells. Results of our experiments demonstrate that this disaccharide is not sufficient for blocking binding of Pap-2 fimbriae to Bowman's capsule but that GalNAc beta 1----3Gal completely blocks Pap-2 adherence to Bowman's capsule. These results indicate that the different hemagglutination capacities of the two clones reflect different receptor specificities and differential tissue tropisms in the urinary tract. These unique receptor specificities may provide uropathogenic strains of Escherichia coli carrying multiple chromosomal copies of pap-like gene clusters with the advantage of increased numbers of binding sites within the urinary tract. This, in turn, might improve the chances of colonization and the establishment of infection.

Full text

PDF

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe C., Schmitz S., Moser I., Boulnois G., High N. J., Orskov I., Orskov F., Jann B., Jann K. Monoclonal antibodies with fimbrial F1C, F12, F13, and F14 specificities obtained with fimbriae from E. coli 04:K12:H-. Microb Pathog. 1987 Jan;2(1):71–77. doi: 10.1016/0882-4010(87)90116-1. [DOI] [PubMed] [Google Scholar]
  2. Arthur M., Campanelli C., Arbeit R. D., Kim C., Steinbach S., Johnson C. E., Rubin R. H., Goldstein R. Structure and copy number of gene clusters related to the pap P-adhesin operon of uropathogenic Escherichia coli. Infect Immun. 1989 Feb;57(2):314–321. doi: 10.1128/iai.57.2.314-321.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Båga M., Göransson M., Normark S., Uhlin B. E. Transcriptional activation of a pap pilus virulence operon from uropathogenic Escherichia coli. EMBO J. 1985 Dec 30;4(13B):3887–3893. doi: 10.1002/j.1460-2075.1985.tb04162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eden C. S., Eriksson B., Hanson L. A. Adhesion of Escherichia coli to human uroepithelial cells in vitro. Infect Immun. 1977 Dec;18(3):767–774. doi: 10.1128/iai.18.3.767-774.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Edén C. S., Eriksson B., Hanson L. A., Jodal U., Kaijser B., Janson G. L., Lindberg U., Olling S. Adhesion to normal human uroepithelial cells of Escherichia coli from children with various forms of urinary tract infection. J Pediatr. 1978 Sep;93(3):398–403. doi: 10.1016/s0022-3476(78)81145-7. [DOI] [PubMed] [Google Scholar]
  6. Enerbäck S., Larsson A. C., Leffler H., Lundell A., de Man P., Nilsson B., Svanborg-Edén C. Binding to galactose alpha 1----4galactose beta-containing receptors as potential diagnostic tool in urinary tract infection. J Clin Microbiol. 1987 Feb;25(2):407–411. doi: 10.1128/jcm.25.2.407-411.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hennigar R. A., Schulte B. A., Spicer S. S. Heterogeneous distribution of glycoconjugates in human kidney tubules. Anat Rec. 1985 Apr;211(4):376–390. doi: 10.1002/ar.1092110403. [DOI] [PubMed] [Google Scholar]
  8. Holthöfer H. Lectin binding sites in kidney. A comparative study of 14 animal species. J Histochem Cytochem. 1983 Apr;31(4):531–537. doi: 10.1177/31.4.6827083. [DOI] [PubMed] [Google Scholar]
  9. Holthöfer H., Virtanen I., Pettersson E., Törnroth T., Alfthan O., Linder E., Miettinen A. Lectins as fluorescence microscopic markers for saccharides in the human kidney. Lab Invest. 1981 Nov;45(5):391–399. [PubMed] [Google Scholar]
  10. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun. 1981 Sep;33(3):933–938. doi: 10.1128/iai.33.3.933-938.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hull R. A., Hull S. I., Falkow S. Frequency of gene sequences necessary for pyelonephritis-associated pili expression among isolates of Enterobacteriaceae from human extraintestinal infections. Infect Immun. 1984 Mar;43(3):1064–1067. doi: 10.1128/iai.43.3.1064-1067.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hull R., Bieler S., Falkow S., Hull S. Chromosomal map position of genes encoding P adhesins in uropathogenic Escherichia coli. Infect Immun. 1986 Feb;51(2):693–695. doi: 10.1128/iai.51.2.693-695.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hull S. I., Bieler S., Hull R. A. Restriction fragment length polymorphism and multiple copies of DNA sequences homologous with probes for P-fimbriae and hemolysin genes among uropathogenic Escherichia coli. Can J Microbiol. 1988 Mar;34(3):307–311. doi: 10.1139/m88-056. [DOI] [PubMed] [Google Scholar]
  14. Hull S., Clegg S., Sanborg Eden C., Hull R. Multiple forms of genes in pyelonephritogenic Escherichia coli encoding adhesins binding globoseries glycolipid receptors. Infect Immun. 1985 Jan;47(1):80–83. doi: 10.1128/iai.47.1.80-83.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Korhonen T. K., Virkola R., Holthöfer H. Localization of binding sites for purified Escherichia coli P fimbriae in the human kidney. Infect Immun. 1986 Nov;54(2):328–332. doi: 10.1128/iai.54.2.328-332.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Korhonen T. K., Väisänen V., Saxén H., Hultberg H., Svenson S. B. P-antigen-recognizing fimbriae from human uropathogenic Escherichia coli strains. Infect Immun. 1982 Jul;37(1):286–291. doi: 10.1128/iai.37.1.286-291.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Källenius G., Svenson S. B., Möllby R., Korhonen T., Winberg J., Cedergren B., Helin I., Hultberg H. Carbohydrate receptor structures recognized by uropathogenic E. coli. Scand J Infect Dis Suppl. 1982;33:52–60. [PubMed] [Google Scholar]
  18. Källenius G., Svenson S., Möllby R., Cedergren B., Hultberg H., Winberg J. Structure of carbohydrate part of receptor on human uroepithelial cells for pyelonephritogenic Escherichia coli. Lancet. 1981 Sep 19;2(8247):604–606. doi: 10.1016/s0140-6736(81)92743-4. [DOI] [PubMed] [Google Scholar]
  19. Lindberg F. P., Lund B., Normark S. Genes of pyelonephritogenic E. coli required for digalactoside-specific agglutination of human cells. EMBO J. 1984 May;3(5):1167–1173. doi: 10.1002/j.1460-2075.1984.tb01946.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lindstedt R., Baker N., Falk P., Hull R., Hull S., Karr J., Leffler H., Svanborg Edén C., Larson G. Binding specificities of wild-type and cloned Escherichia coli strains that recognize globo-A. Infect Immun. 1989 Nov;57(11):3389–3394. doi: 10.1128/iai.57.11.3389-3394.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lund B., Lindberg F. P., Båga M., Normark S. Globoside-specific adhesins of uropathogenic Escherichia coli are encoded by similar trans-complementable gene clusters. J Bacteriol. 1985 Jun;162(3):1293–1301. doi: 10.1128/jb.162.3.1293-1301.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lund B., Lindberg F., Marklund B. I., Normark S. The PapG protein is the alpha-D-galactopyranosyl-(1----4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5898–5902. doi: 10.1073/pnas.84.16.5898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lund B., Lindberg F., Normark S. Structure and antigenic properties of the tip-located P pilus proteins of uropathogenic Escherichia coli. J Bacteriol. 1988 Apr;170(4):1887–1894. doi: 10.1128/jb.170.4.1887-1894.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lund B., Marklund B. I., Strömberg N., Lindberg F., Karlsson K. A., Normark S. Uropathogenic Escherichia coli can express serologically identical pili of different receptor binding specificities. Mol Microbiol. 1988 Mar;2(2):255–263. doi: 10.1111/j.1365-2958.1988.tb00027.x. [DOI] [PubMed] [Google Scholar]
  25. Norgren M., Normark S., Lark D., O'Hanley P., Schoolnik G., Falkow S., Svanborg-Edén C., Båga M., Uhlin B. E. Mutations in E coli cistrons affecting adhesion to human cells do not abolish Pap pili fiber formation. EMBO J. 1984 May;3(5):1159–1165. doi: 10.1002/j.1460-2075.1984.tb01945.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Normark S., Lark D., Hull R., Norgren M., Båga M., O'Hanley P., Schoolnik G., Falkow S. Genetics of digalactoside-binding adhesin from a uropathogenic Escherichia coli strain. Infect Immun. 1983 Sep;41(3):942–949. doi: 10.1128/iai.41.3.942-949.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nowicki B., Rhen M., Väisänen-Rhen V., Pere A., Korhonen T. K. Immunofluorescence study of fimbrial phase variation in Escherichia coli KS71. J Bacteriol. 1984 Nov;160(2):691–695. doi: 10.1128/jb.160.2.691-695.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nowicki B., Truong L., Moulds J., Hull R. Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. Am J Pathol. 1988 Oct;133(1):1–4. [PMC free article] [PubMed] [Google Scholar]
  29. Orskov I., Orskov F. Serology of Escherichia coli fimbriae. Prog Allergy. 1983;33:80–105. [PubMed] [Google Scholar]
  30. Pere A., Selander R. K., Korhonen T. K. Characterization of P fimbriae on O1, O7, O75, rough, and nontypable strains of Escherichia coli. Infect Immun. 1988 May;56(5):1288–1294. doi: 10.1128/iai.56.5.1288-1294.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pere A., Väisänen-Rhen V., Rhen M., Tenhunen J., Korhonen T. K. Analysis of P fimbriae on Escherichia coli O2, O4, and O6 strains by immunoprecipitation. Infect Immun. 1986 Feb;51(2):618–625. doi: 10.1128/iai.51.2.618-625.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Senior D., Baker N., Cedergren B., Falk P., Larson G., Lindstedt R., Edén C. S. Globo-A--a new receptor specificity for attaching Escherichia coli. FEBS Lett. 1988 Sep 12;237(1-2):123–127. doi: 10.1016/0014-5793(88)80184-4. [DOI] [PubMed] [Google Scholar]
  33. Truong L. D., Phung V. T., Yoshikawa Y., Mattioli C. A. Glycoconjugates in normal human kidney. A histochemical study using 13 biotinylated lectins. Histochemistry. 1988;90(1):51–60. doi: 10.1007/BF00495707. [DOI] [PubMed] [Google Scholar]
  34. Uhlin B. E., Norgren M., Båga M., Normark S. Adhesion to human cells by Escherichia coli lacking the major subunit of a digalactoside-specific pilus-adhesin. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1800–1804. doi: 10.1073/pnas.82.6.1800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Virkola R., Westerlund B., Holthöfer H., Parkkinen J., Kekomäki M., Korhonen T. K. Binding characteristics of Escherichia coli adhesins in human urinary bladder. Infect Immun. 1988 Oct;56(10):2615–2622. doi: 10.1128/iai.56.10.2615-2622.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wray S. K., Hull S. I., Cook R. G., Barrish J., Hull R. A. Identification and characterization of a uroepithelial cell adhesin from a uropathogenic isolate of Proteus mirabilis. Infect Immun. 1986 Oct;54(1):43–49. doi: 10.1128/iai.54.1.43-49.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES