Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1985 Jun;162(3):1293–1301. doi: 10.1128/jb.162.3.1293-1301.1985

Globoside-specific adhesins of uropathogenic Escherichia coli are encoded by similar trans-complementable gene clusters.

B Lund, F P Lindberg, M Båga, S Normark
PMCID: PMC215918  PMID: 2860097

Abstract

Uropathogenic Escherichia coli frequently express globoside-specific adhesins, shown to mediate binding to uroepithelial cells. For one gene cluster pap, it recently has been demonstrated that globoside binding is not dependent on expression of the pilus subunit gene papA. Instead, two other pap genes papF and papG are specifically required for globoside binding (F. P. Lindberg et al., EMBO J. 3:1167-1173, 1984). By restriction enzyme mapping, DNA hybridization, DNA sequencing, and protein expression in minicells, we show that three gene clusters encoding globoside binding have a very similar structure and gene organization, although they were cloned from different E. coli isolates. Major differences between the adhesin clones were restricted to the central part of the pilin gene (papA) and to one of the two adhesin gene (papG). The three functional units required for biogenesis of globoside-binding pili, i.e., pilin synthesis, pilin export, and pilin assembly, as well as expression of adhesion function, were all trans complementable among the gene clusters.

Full text

PDF
1293

Images in this article

1297Image
on p.1297
1298Image
on p.1298

Selected References

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

  1. Adler H. I., Fisher W. D., Cohen A., Hardigree A. A. MINIATURE escherichia coli CELLS DEFICIENT IN DNA. Proc Natl Acad Sci U S A. 1967 Feb;57(2):321–326. doi: 10.1073/pnas.57.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akusjärvi G., Pettersson U. Sequence analysis of adenovirus DNA. I. Nucleotide sequence at the carboxy-terminal end of the gene for adenovirus type 2 hexon. Virology. 1978 Dec;91(2):477–480. doi: 10.1016/0042-6822(78)90394-x. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [DOI] [PubMed] [Google Scholar]
  5. Berger H., Hacker J., Juarez A., Hughes C., Goebel W. Cloning of the chromosomal determinants encoding hemolysin production and mannose-resistant hemagglutination in Escherichia coli. J Bacteriol. 1982 Dec;152(3):1241–1247. doi: 10.1128/jb.152.3.1241-1247.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bergström S., Lindberg F. P., Olsson O., Normark S. Comparison of the overlapping frd and ampC operons of Escherichia coli with the corresponding DNA sequences in other gram-negative bacteria. J Bacteriol. 1983 Sep;155(3):1297–1305. doi: 10.1128/jb.155.3.1297-1305.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Brinton C. C., Jr The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans N Y Acad Sci. 1965 Jun;27(8):1003–1054. doi: 10.1111/j.2164-0947.1965.tb02342.x. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Casadaban M. J., Martinez-Arias A., Shapira S. K., Chou J. Beta-galactosidase gene fusions for analyzing gene expression in escherichia coli and yeast. Methods Enzymol. 1983;100:293–308. doi: 10.1016/0076-6879(83)00063-4. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Clegg S. Cloning of genes determining the production of mannose-resistant fimbriae in a uropathogenic strain of Escherichia coli belonging to serogroup O6. Infect Immun. 1982 Nov;38(2):739–744. doi: 10.1128/iai.38.2.739-744.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Clegg S., Pierce J. K. Organization of genes responsible for the production of mannose-resistant fimbriae of a uropathogenic Escherichia coli isolate. Infect Immun. 1983 Dec;42(3):900–906. doi: 10.1128/iai.42.3.900-906.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  17. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  18. Grosveld F. G., Dahl H. H., de Boer E., Flavell R. A. Isolation of beta-globin-related genes from a human cosmid library. Gene. 1981 Apr;13(3):227–237. doi: 10.1016/0378-1119(81)90028-7. [DOI] [PubMed] [Google Scholar]
  19. Hagberg L., Jodal U., Korhonen T. K., Lidin-Janson G., Lindberg U., Svanborg Edén C. Adhesion, hemagglutination, and virulence of Escherichia coli causing urinary tract infections. Infect Immun. 1981 Feb;31(2):564–570. doi: 10.1128/iai.31.2.564-570.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Low D., David V., Lark D., Schoolnik G., Falkow S. Gene clusters governing the production of hemolysin and mannose-resistant hemagglutination are closely linked in Escherichia coli serotype O4 and O6 isolates from urinary tract infections. Infect Immun. 1984 Jan;43(1):353–358. doi: 10.1128/iai.43.1.353-358.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lund B., Edlund T., Lindenmaier W., Ny T., Collins J., Lundgren E., von Gabain A. Novel cluster of alpha-interferon gene sequences in a placental cosmid DNA library. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2435–2439. doi: 10.1073/pnas.81.8.2435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Meyer T. F., Mlawer N., So M. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell. 1982 Aug;30(1):45–52. doi: 10.1016/0092-8674(82)90010-1. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Ricca G. A., Taylor J. M., Kalinyak J. E. Simple rapid method for the synthesis of radioactively labeled cDNA hybridization probes utilizing bacteriophage M13mp7. Proc Natl Acad Sci U S A. 1982 Feb;79(3):724–728. doi: 10.1073/pnas.79.3.724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rothbard J. B., Fernandez R., Schoolnik G. K. Strain-specific and common epitopes of gonococcal pili. J Exp Med. 1984 Jul 1;160(1):208–221. doi: 10.1084/jem.160.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Schoolnik G. K., Fernandez R., Tai J. Y., Rothbard J., Gotschlich E. C. Gonococcal pili. Primary structure and receptor binding domain. J Exp Med. 1984 May 1;159(5):1351–1370. doi: 10.1084/jem.159.5.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Thompson R., Achtman M. The control region of the F sex factor DNA transfer cistrons: restriction mapping and DNA cloning. Mol Gen Genet. 1978 Oct 24;165(3):295–304. doi: 10.1007/BF00332530. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Väisänen V., Elo J., Tallgren L. G., Siitonen A., Mäkelä P. H., Svanborg-Edén C., Källenius G., Svenson S. B., Hultberg H., Korhonen T. Mannose-resistant haemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet. 1981 Dec 19;2(8260-61):1366–1369. doi: 10.1016/s0140-6736(81)92796-3. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. van Die I., van Megen I., Hoekstra W., Bergmans H. Molecular organisation of the genes involved in the production of F7(2) fimbriae, causing mannose-resistant haemagglutination, of a uropathogenic Escherichia coli 06:K2:H1:F7 strain. Mol Gen Genet. 1984;194(3):528–533. doi: 10.1007/BF00425570. [DOI] [PubMed] [Google Scholar]
  46. van der Bosch J. F., Verboom-Sohmer U., Postma P., de Graaff J., MacLaren D. M. Mannose-sensitive and mannose-resistant adherence to human uroepithelial cells and urinary virulence of Escherichia coli. Infect Immun. 1980 Jul;29(1):226–233. doi: 10.1128/iai.29.1.226-233.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES