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
. 1986 Mar;83(6):1891–1895. doi: 10.1073/pnas.83.6.1891

Gene products specifying adhesion of uropathogenic Escherichia coli are minor components of pili.

F Lindberg, B Lund, S Normark
PMCID: PMC323190  PMID: 2869489

Abstract

The papE, papF, and papG genes of uropathogenic Escherichia coli are dispensable for the synthesis and assembly of pili associated with pyelonephritis, called Pap pili. Phenotypically, papF and papG mediate digalactoside [alpha-D-Galp-(1----4)-beta-D-Galp)-specific adhesion. Although whole bacterial cells of a papE mutant bind to this receptor, purified pili from such a mutant do not. This is in contrast to pili purified from the wild type, which bind specifically. The DNA sequences of the papE and papF genes are presented, together with the deduced primary structure of the gene products. Both proteins have most of the features characteristic of Escherichia coli type 1 and Pap pilins. The PapE protein can be detected in the purified wild-type pilus by NaDodSO4/polyacrylamide gel electrophoresis followed by silver staining or by autoradiography of gels to which radioiodinated pili have been applied. In rabbits immunized with purified Pap pili, antibodies specific for both PapE and PapF are produced. We propose that PapE and PapF are minor pilins in the Pap pilus.

Full text

PDF
1892

Images in this article

1894Image
on p.1894

Selected References

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

  1. BERTANI G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol. 1951 Sep;62(3):293–300. doi: 10.1128/jb.62.3.293-300.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Båga M., Normark S., Hardy J., O'Hanley P., Lark D., Olsson O., Schoolnik G., Falkow S. Nucleotide sequence of the papA gene encoding the Pap pilus subunit of human uropathogenic Escherichia coli. J Bacteriol. 1984 Jan;157(1):330–333. doi: 10.1128/jb.157.1.330-333.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Grundström T., Jaurin B., Edlund T., Normark S. Physical mapping and expression of hybrid plasmids carrying chromosomal beta-lactamase genes of Escherichia coli K-12. J Bacteriol. 1980 Sep;143(3):1127–1134. doi: 10.1128/jb.143.3.1127-1134.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Jones G. W., Isaacson R. E. Proteinaceous bacterial adhesins and their receptors. Crit Rev Microbiol. 1983;10(3):229–260. doi: 10.3109/10408418209113564. [DOI] [PubMed] [Google Scholar]
  8. Klemm P. The fimA gene encoding the type-1 fimbrial subunit of Escherichia coli. Nucleotide sequence and primary structure of the protein. Eur J Biochem. 1984 Sep 3;143(2):395–399. doi: 10.1111/j.1432-1033.1984.tb08386.x. [DOI] [PubMed] [Google Scholar]
  9. Korhonen T. K., Nurmiaho E. L., Ranta H., Edén C. S. New Method for isolation of immunologically pure pili from Escherichia coli. Infect Immun. 1980 Feb;27(2):569–575. doi: 10.1128/iai.27.2.569-575.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leffler H., Svanborg-Edén C. Glycolipid receptors for uropathogenic Escherichia coli on human erythrocytes and uroepithelial cells. Infect Immun. 1981 Dec;34(3):920–929. doi: 10.1128/iai.34.3.920-929.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Markwell M. A., Fox C. F. Surface-specific iodination of membrane proteins of viruses and eucaryotic cells using 1,3,4,6-tetrachloro-3alpha,6alpha-diphenylglycoluril. Biochemistry. 1978 Oct 31;17(22):4807–4817. doi: 10.1021/bi00615a031. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Oakley B. R., Kirsch D. R., Morris N. R. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem. 1980 Jul 1;105(2):361–363. doi: 10.1016/0003-2697(80)90470-4. [DOI] [PubMed] [Google Scholar]
  21. Orndorff P. E., Falkow S. Nucleotide sequence of pilA, the gene encoding the structural component of type 1 pili in Escherichia coli. J Bacteriol. 1985 Apr;162(1):454–457. doi: 10.1128/jb.162.1.454-457.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. Smith H. O., Birnstiel M. L. A simple method for DNA restriction site mapping. Nucleic Acids Res. 1976 Sep;3(9):2387–2398. doi: 10.1093/nar/3.9.2387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Staden R. A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res. 1980 Aug 25;8(16):3673–3694. doi: 10.1093/nar/8.16.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Sweet R. M., Eisenberg D. Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. J Mol Biol. 1983 Dec 25;171(4):479–488. doi: 10.1016/0022-2836(83)90041-4. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. van Die I., van Geffen B., Hoekstra W., Bergmans H. Type 1C fimbriae of a uropathogenic Escherichia coli strain: cloning and characterization of the genes involved in the expression of the 1C antigen and nucleotide sequence of the subunit gene. Gene. 1985;34(2-3):187–196. doi: 10.1016/0378-1119(85)90127-1. [DOI] [PubMed] [Google Scholar]
  32. 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