Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Aug;84(16):5898–5902. doi: 10.1073/pnas.84.16.5898

The PapG protein is the alpha-D-galactopyranosyl-(1----4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli.

B Lund, F Lindberg, B I Marklund, S Normark
PMCID: PMC298970  PMID: 2886993

Abstract

Uropathogenic Escherichia coli adhere to uroepithelial cells by their digalactoside alpha-D-galactopyranosyl-(1----4)-beta-D-galactopyranose [alpha-D-Galp-(1----4)-beta-D-Galp or Gal alpha (1----4)Gal]-binding pili, which are composed of repeating identical subunits. The major subunit (PapA) of these pili is not required for binding, but the papF and papG gene products are essential for adhesion. Transcomplementation analysis between the pap gene cluster and a related gene cluster encoding a different binding specificity showed that PapG and not PapF is the Gal alpha (1----4)Gal-specific adhesin. Antibodies against PapG were obtained upon immunizing with whole Pap pili, showing that the adhesin is a pilus component. Antisera specific for different Pap proteins were used to demonstrate that a pilin protein, either PapA or PapE, together with both PapG and PapF, must be exposed on the cell surface to allow E. coli to bind. The DNA sequence of the papG gene is presented, and the deduced primary structure showed similarities both to the B-chain sequence of the digalactoside-binding Shigella toxin and to established amino acid sequences of pilins.

Full text

PDF
5902

Selected References

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

  1. Bock K., Breimer M. E., Brignole A., Hansson G. C., Karlsson K. A., Larson G., Leffler H., Samuelsson B. E., Strömberg N., Edén C. S. Specificity of binding of a strain of uropathogenic Escherichia coli to Gal alpha 1----4Gal-containing glycosphingolipids. J Biol Chem. 1985 Jul 15;260(14):8545–8551. [PubMed] [Google Scholar]
  2. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  3. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  4. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1986 Jan 10;14(1):11–15. doi: 10.1093/nar/14.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hagberg L., Engberg I., Freter R., Lam J., Olling S., Svanborg Edén C. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect Immun. 1983 Apr;40(1):273–283. doi: 10.1128/iai.40.1.273-283.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hagberg L., Hull R., Hull S., Falkow S., Freter R., Svanborg Edén C. Contribution of adhesion to bacterial persistence in the mouse urinary tract. Infect Immun. 1983 Apr;40(1):265–272. doi: 10.1128/iai.40.1.265-272.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Harr R., Fällman P., Häggström M., Wahlström L., Gustafsson P. GENEUS, a computer system for DNA and protein sequence analysis containing an information retrieval system for the EMBL data library. Nucleic Acids Res. 1986 Jan 10;14(1):273–284. doi: 10.1093/nar/14.1.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Inouye M., Halegoua S. Secretion and membrane localization of proteins in Escherichia coli. CRC Crit Rev Biochem. 1980;7(4):339–371. doi: 10.3109/10409238009105465. [DOI] [PubMed] [Google Scholar]
  11. Jacewicz M., Clausen H., Nudelman E., Donohue-Rolfe A., Keusch G. T. Pathogenesis of shigella diarrhea. XI. Isolation of a shigella toxin-binding glycolipid from rabbit jejunum and HeLa cells and its identification as globotriaosylceramide. J Exp Med. 1986 Jun 1;163(6):1391–1404. doi: 10.1084/jem.163.6.1391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Klemm P. Primary structure of the CFA1 fimbrial protein from human enterotoxigenic Escherichia coli strains. Eur J Biochem. 1982 May 17;124(2):339–348. doi: 10.1111/j.1432-1033.1982.tb06597.x. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Källenius G., Möllby R., Svenson S. B., Helin I., Hultberg H., Cedergren B., Winberg J. Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet. 1981 Dec 19;2(8260-61):1369–1372. doi: 10.1016/s0140-6736(81)92797-5. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Lindberg F., Lund B., Normark S. Gene products specifying adhesion of uropathogenic Escherichia coli are minor components of pili. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1891–1895. doi: 10.1073/pnas.83.6.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lindberg F., Westman L., Normark S. Regulatory components in Citrobacter freundii ampC beta-lactamase induction. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4620–4624. doi: 10.1073/pnas.82.14.4620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. O'Hanley P., Lark D., Normark S., Falkow S., Schoolnik G. K. Mannose-sensitive and Gal-Gal binding Escherichia coli pili from recombinant strains. Chemical, functional, and serological properties. J Exp Med. 1983 Nov 1;158(5):1713–1719. doi: 10.1084/jem.158.5.1713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Hanley P., Low D., Romero I., Lark D., Vosti K., Falkow S., Schoolnik G. Gal-Gal binding and hemolysin phenotypes and genotypes associated with uropathogenic Escherichia coli. N Engl J Med. 1985 Aug 15;313(7):414–420. doi: 10.1056/NEJM198508153130704. [DOI] [PubMed] [Google Scholar]
  25. Rhen M., van Die I., Rhen V., Bergmans H. Comparison of the nucleotide sequences of the genes encoding the KS71A and F7(1) fimbrial antigens of uropathogenic Escherichia coli. Eur J Biochem. 1985 Sep 16;151(3):573–577. doi: 10.1111/j.1432-1033.1985.tb09142.x. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Seidah N. G., Donohue-Rolfe A., Lazure C., Auclair F., Keusch G. T., Chrétien M. Complete amino acid sequence of Shigella toxin B-chain. A novel polypeptide containing 69 amino acids and one disulfide bridge. J Biol Chem. 1986 Oct 25;261(30):13928–13931. [PubMed] [Google Scholar]
  28. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Svenson S. B., Hultberg H., Källenius G., Korhonen T. K., Möllby R., Winberg J. P-fimbriae of pyelonephritogenic Escherichia coli: identification and chemical characterization of receptors. Infection. 1983 Jan-Feb;11(1):61–67. doi: 10.1007/BF01651362. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Van Die I., Van Megen I., Zuidweg E., Hoekstra W., De Ree H., Van den Bosch H., Bergmans H. Functional relationship among the gene clusters encoding F7(1), F7(2), F9, and F11 fimbriae of human uropathogenic Escherichia coli. J Bacteriol. 1986 Jul;167(1):407–410. doi: 10.1128/jb.167.1.407-410.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van Die I., Bergmans H. Nucleotide sequence of the gene encoding the F72 fimbrial subunit of a uropathogenic Escherichia coli strain. Gene. 1984 Dec;32(1-2):83–90. doi: 10.1016/0378-1119(84)90035-0. [DOI] [PubMed] [Google Scholar]
  34. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES