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. 1995 Dec;63(12):4849–4856. doi: 10.1128/iai.63.12.4849-4856.1995

Genes for CS2 pili of enterotoxigenic Escherichia coli and their interchangeability with those for CS1 pili.

B J Froehlich 1, A Karakashian 1, H Sakellaris 1, J R Scott 1
PMCID: PMC173694  PMID: 7591145

Abstract

We have cloned and sequenced the DNA needed for production of CS2 pili in Escherichia coli K-12. The four open reading frames, cotB, cotA, cotC, and cotD, show homology with the genes needed for production of CS1 and CFA/I pili, which are also found on enterotoxigenic E. coli associated with human diarrheal disease. We also report that CotA plus CotB interact with the CS1 gene products CooC and CooD to form pili that can be visualized by electron microscopy and, conversely, that the CS1 gene products CooA and CooB interact with CotC and CotD to form pili.

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Selected References

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  1. Caron J., Coffield L. M., Scott J. R. A plasmid-encoded regulatory gene, rns, required for expression of the CS1 and CS2 adhesins of enterotoxigenic Escherichia coli. Proc Natl Acad Sci U S A. 1989 Feb;86(3):963–967. doi: 10.1073/pnas.86.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Caron J., Maneval D. R., Kaper J. B., Scott J. R. Association of rns homologs with colonization factor antigens in clinical Escherichia coli isolates. Infect Immun. 1990 Oct;58(10):3442–3444. doi: 10.1128/iai.58.10.3442-3444.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Caron J., Scott J. R. A rns-like regulatory gene for colonization factor antigen I (CFA/I) that controls expression of CFA/I pilin. Infect Immun. 1990 Apr;58(4):874–878. doi: 10.1128/iai.58.4.874-878.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Casadaban M. J. Regulation of the regulatory gene for the arabinose pathway, araC. J Mol Biol. 1976 Jul 5;104(3):557–566. doi: 10.1016/0022-2836(76)90120-0. [DOI] [PubMed] [Google Scholar]
  5. Dodson K. W., Jacob-Dubuisson F., Striker R. T., Hultgren S. J. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3670–3674. doi: 10.1073/pnas.90.8.3670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Evans D. G., Evans D. J., Jr New surface-associated heat-labile colonization factor antigen (CFA/II) produced by enterotoxigenic Escherichia coli of serogroups O6 and O8. Infect Immun. 1978 Aug;21(2):638–647. doi: 10.1128/iai.21.2.638-647.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Froehlich B. J., Karakashian A., Melsen L. R., Wakefield J. C., Scott J. R. CooC and CooD are required for assembly of CS1 pili. Mol Microbiol. 1994 May;12(3):387–401. doi: 10.1111/j.1365-2958.1994.tb01028.x. [DOI] [PubMed] [Google Scholar]
  9. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem. 1988;57:199–233. doi: 10.1146/annurev.bi.57.070188.001215. [DOI] [PubMed] [Google Scholar]
  10. Hamers A. M., Pel H. J., Willshaw G. A., Kusters J. G., van der Zeijst B. A., Gaastra W. The nucleotide sequence of the first two genes of the CFA/I fimbrial operon of human enterotoxigenic Escherichia coli. Microb Pathog. 1989 Apr;6(4):297–309. doi: 10.1016/0882-4010(89)90103-4. [DOI] [PubMed] [Google Scholar]
  11. Hawley D. K., McClure W. R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. doi: 10.1093/nar/11.8.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hohn B., Collins J. A small cosmid for efficient cloning of large DNA fragments. Gene. 1980 Nov;11(3-4):291–298. doi: 10.1016/0378-1119(80)90069-4. [DOI] [PubMed] [Google Scholar]
  13. Hultgren S. J., Abraham S., Caparon M., Falk P., St Geme J. W., 3rd, Normark S. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell. 1993 Jun 4;73(5):887–901. doi: 10.1016/0092-8674(93)90269-v. [DOI] [PubMed] [Google Scholar]
  14. Jap B. K., Walian P. J. Biophysics of the structure and function of porins. Q Rev Biophys. 1990 Nov;23(4):367–403. doi: 10.1017/s003358350000559x. [DOI] [PubMed] [Google Scholar]
  15. Jones C. H., Pinkner J. S., Nicholes A. V., Slonim L. N., Abraham S. N., Hultgren S. J. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8397–8401. doi: 10.1073/pnas.90.18.8397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jordi B. J., Willshaw G. A., van der Zeijst B. A., Gaastra W. The complete nucleotide sequence of region 1 of the CFA/I fimbrial operon of human enterotoxigenic Escherichia coli. DNA Seq. 1992;2(4):257–263. doi: 10.3109/10425179209020811. [DOI] [PubMed] [Google Scholar]
  17. Jordi B. J., van Vliet A. H., Willshaw G. A., van der Zeijst B. A., Gaastra W. Analysis of the first two genes of the CS1 fimbrial operon in human enterotoxigenic Escherichia coli of serotype 0139:H28. FEMS Microbiol Lett. 1991 May 15;64(2-3):265–270. doi: 10.1016/0378-1097(91)90607-c. [DOI] [PubMed] [Google Scholar]
  18. Karlyshev A. V., Galyov E. E., Smirnov OYu, Guzayev A. P., Abramov V. M., Zav'yalov V. P. A new gene of the f1 operon of Y. pestis involved in the capsule biogenesis. FEBS Lett. 1992 Feb 3;297(1-2):77–80. doi: 10.1016/0014-5793(92)80331-a. [DOI] [PubMed] [Google Scholar]
  19. Klemm P., Jørgensen B. J., Kreft B., Christiansen G. The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs. J Bacteriol. 1995 Feb;177(3):621–627. doi: 10.1128/jb.177.3.621-627.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levine M. M., Ristaino P., Marley G., Smyth C., Knutton S., Boedeker E., Black R., Young C., Clements M. L., Cheney C. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. Infect Immun. 1984 May;44(2):409–420. doi: 10.1128/iai.44.2.409-420.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McConnell M. M., Chart H., Rowe B. Antigenic homology within human enterotoxigenic Escherichia coli fimbrial colonization factor antigens: CFA/I, coli-surface-associated antigens (CS)1, CS2, CS4 and CS17. FEMS Microbiol Lett. 1989 Oct 1;52(1-2):105–108. doi: 10.1016/0378-1097(89)90179-1. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Nikaido H., Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 1985 Mar;49(1):1–32. doi: 10.1128/mr.49.1.1-32.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ohtsubo H., Ohtsubo E. Nucleotide sequence of an insertion element, IS1. Proc Natl Acad Sci U S A. 1978 Feb;75(2):615–619. doi: 10.1073/pnas.75.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Perez-Casal J., Swartley J. S., Scott J. R. Gene encoding the major subunit of CS1 pili of human enterotoxigenic Escherichia coli. Infect Immun. 1990 Nov;58(11):3594–3600. doi: 10.1128/iai.58.11.3594-3600.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roosendaal B., de Graaf F. K. The nucleotide sequence of the fanD gene encoding the large outer membrane protein involved in the biosynthesis of K99 fimbriae. Nucleic Acids Res. 1989 Feb 11;17(3):1263–1263. doi: 10.1093/nar/17.3.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rost B., Sander C. Jury returns on structure prediction. Nature. 1992 Dec 10;360(6404):540–540. doi: 10.1038/360540b0. [DOI] [PubMed] [Google Scholar]
  28. Rost B., Sander C. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993 Jul 20;232(2):584–599. doi: 10.1006/jmbi.1993.1413. [DOI] [PubMed] [Google Scholar]
  29. Russell P. W., Orndorff P. E. Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding. J Bacteriol. 1992 Sep;174(18):5923–5935. doi: 10.1128/jb.174.18.5923-5935.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sander C., Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins. 1991;9(1):56–68. doi: 10.1002/prot.340090107. [DOI] [PubMed] [Google Scholar]
  31. Savelkoul P. H., Willshaw G. A., McConnell M. M., Smith H. R., Hamers A. M., van der Zeijst B. A., Gaastra W. Expression of CFA/I fimbriae is positively regulated. Microb Pathog. 1990 Feb;8(2):91–99. doi: 10.1016/0882-4010(90)90073-y. [DOI] [PubMed] [Google Scholar]
  32. Scott J. R. A turbid plaque-forming mutant of phage P1 that cannot lysogenize Escherichia coli. Virology. 1974 Dec;62(2):344–349. doi: 10.1016/0042-6822(74)90397-3. [DOI] [PubMed] [Google Scholar]
  33. Scott J. R., Wakefield J. C., Russell P. W., Orndorff P. E., Froehlich B. J. CooB is required for assembly but not transport of CS1 pilin. Mol Microbiol. 1992 Feb;6(3):293–300. doi: 10.1111/j.1365-2958.1992.tb01471.x. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Smyth C. J. Two mannose-resistant haemagglutinins on enterotoxigenic Escherichia coli of serotype O6:K15:H16 or H-isolated from travellers' and infantile diarrhoea. J Gen Microbiol. 1982 Sep;128(9):2081–2096. doi: 10.1099/00221287-128-9-2081. [DOI] [PubMed] [Google Scholar]
  36. Sommerfelt H., Grewal H. M., Svennerholm A. M., Gaastra W., Flood P. R., Viboud G., Bhan M. K. Genetic relationship of putative colonization factor O166 to colonization factor antigen I and coli surface antigen 4 of enterotoxigenic Escherichia coli. Infect Immun. 1992 Sep;60(9):3799–3806. doi: 10.1128/iai.60.9.3799-3806.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Takeshita S., Sato M., Toba M., Masahashi W., Hashimoto-Gotoh T. High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene. 1987;61(1):63–74. doi: 10.1016/0378-1119(87)90365-9. [DOI] [PubMed] [Google Scholar]
  38. Timmerman K. P., Tu C. P. Complete sequence of IS3. Nucleic Acids Res. 1985 Mar 25;13(6):2127–2139. doi: 10.1093/nar/13.6.2127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Willshaw G. A., McConnell M. M., Smith H. R., Rowe B. Structural and regulatory genes for coli surface associated antigen 4 (CS4) are encoded by separate plasmids in enterotoxigenic Escherichia coli strains of serotype 0.25.H42. FEMS Microbiol Lett. 1990 Mar 15;56(3):255–260. [PubMed] [Google Scholar]
  40. Willshaw G. A., Smith H. R., McConnell M. M., Rowe B. Cloning of regulator genes controlling fimbrial production by enterotoxigenic Escherichia coli. FEMS Microbiol Lett. 1991 Aug 1;66(2):125–129. doi: 10.1016/0378-1097(91)90320-a. [DOI] [PubMed] [Google Scholar]
  41. Wolf M. K., Andrews G. P., Tall B. D., McConnell M. M., Levine M. M., Boedeker E. C. Characterization of CS4 and CS6 antigenic components of PCF8775, a putative colonization factor complex from enterotoxigenic Escherichia coli E8775. Infect Immun. 1989 Jan;57(1):164–173. doi: 10.1128/iai.57.1.164-173.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. de Graaf F. K. Genetics of adhesive fimbriae of intestinal Escherichia coli. Curr Top Microbiol Immunol. 1990;151:29–53. doi: 10.1007/978-3-642-74703-8_2. [DOI] [PubMed] [Google Scholar]

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