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. 1992 Jul;11(7):2627–2632. doi: 10.1002/j.1460-2075.1992.tb05328.x

The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli.

B J Jordi 1, B Dagberg 1, L A de Haan 1, A M Hamers 1, B A van der Zeijst 1, W Gaastra 1, B E Uhlin 1
PMCID: PMC556738  PMID: 1378396

Abstract

CFA/I fimbriae of enterotoxigenic Escherichia coli are expressed at 37 degrees C and not at 20 degrees C. Expression of CFA/I fimbriae requires two DNA regions (regions 1 and 2) which are separated by 40 kb on the wild type plasmid. Region 2 encodes a protein (CfaD) which activates the promoter in region 1. We investigated whether the histone-like protein H-NS (H1) of E.coli is involved in the temperature regulated expression of CFA/I fimbriae. As demonstrated recently with other temperature regulated genes, a mutation in the gene coding for this nucleoid-associated H-NS (H1) protein resulted in derepression of CFA/I expression. CFA/I fimbriae were now expressed both at 20 degrees C and 37 degrees C. More strinkingly, the positive regulator CfaD was not needed for CFA/I expression in an H-NS- strain. This indicates that CfaD diminishes an inhibitory effect of the H-NS nucleoid-associated protein. We also showed that in the H-NS- strain the CfaD protein still has a positive effect on the transcription of CFA/I.

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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. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  3. Cravioto A., Scotland S. M., Rowe B. Hemagglutination activity and colonization factor antigens I and II in enterotoxigenic and non-enterotoxigenic strains of Escherichia coli isolated from humans. Infect Immun. 1982 Apr;36(1):189–197. doi: 10.1128/iai.36.1.189-197.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Defez R., De Felice M. Cryptic operon for beta-glucoside metabolism in Escherichia coli K12: genetic evidence for a regulatory protein. Genetics. 1981 Jan;97(1):11–25. doi: 10.1093/genetics/97.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dorman C. J. DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Infect Immun. 1991 Mar;59(3):745–749. doi: 10.1128/iai.59.3.745-749.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dorman C. J., Ni Bhriain N., Higgins C. F. DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature. 1990 Apr 19;344(6268):789–792. doi: 10.1038/344789a0. [DOI] [PubMed] [Google Scholar]
  7. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Evans D. G., Silver R. P., Evans D. J., Jr, Chase D. G., Gorbach S. L. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. doi: 10.1128/iai.12.3.656-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gaastra W., Jordi B. J., Mul E. M., Hamers A. M., McConnell M. M., Willshaw G. A., Smith H. R., van der Zeijst B. A. A silent regulatory gene cfaD' on region 1 of the CFA/I plasmid NTP 113 of enterotoxigenic Escherichia coli. Microb Pathog. 1990 Oct;9(4):285–291. doi: 10.1016/0882-4010(90)90017-k. [DOI] [PubMed] [Google Scholar]
  11. Goldstein E., Drlica K. Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4046–4050. doi: 10.1073/pnas.81.13.4046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Göransson M., Forsman K., Uhlin B. E. Regulatory genes in the thermoregulation of Escherichia coli pili gene transcription. Genes Dev. 1989 Jan;3(1):123–130. doi: 10.1101/gad.3.1.123. [DOI] [PubMed] [Google Scholar]
  13. Göransson M., Sondén B., Nilsson P., Dagberg B., Forsman K., Emanuelsson K., Uhlin B. E. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature. 1990 Apr 12;344(6267):682–685. doi: 10.1038/344682a0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Higgins C. F., Dorman C. J., Stirling D. A., Waddell L., Booth I. R., May G., Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. doi: 10.1016/0092-8674(88)90470-9. [DOI] [PubMed] [Google Scholar]
  16. Higgins C. F., Hinton J. C., Hulton C. S., Owen-Hughes T., Pavitt G. D., Seirafi A. Protein H1: a role for chromatin structure in the regulation of bacterial gene expression and virulence? Mol Microbiol. 1990 Dec;4(12):2007–2012. doi: 10.1111/j.1365-2958.1990.tb00559.x. [DOI] [PubMed] [Google Scholar]
  17. Hulton C. S., Seirafi A., Hinton J. C., Sidebotham J. M., Waddell L., Pavitt G. D., Owen-Hughes T., Spassky A., Buc H., Higgins C. F. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell. 1990 Nov 2;63(3):631–642. doi: 10.1016/0092-8674(90)90458-q. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  21. Liu L. F., Wang J. C. Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7024–7027. doi: 10.1073/pnas.84.20.7024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maurelli A. T. Temperature regulation of virulence genes in pathogenic bacteria: a general strategy for human pathogens? Microb Pathog. 1989 Jul;7(1):1–10. doi: 10.1016/0882-4010(89)90106-x. [DOI] [PubMed] [Google Scholar]
  23. May G., Dersch P., Haardt M., Middendorf A., Bremer E. The osmZ (bglY) gene encodes the DNA-binding protein H-NS (H1a), a component of the Escherichia coli K12 nucleoid. Mol Gen Genet. 1990 Oct;224(1):81–90. doi: 10.1007/BF00259454. [DOI] [PubMed] [Google Scholar]
  24. Mooi F. R., de Graaf F. K. Molecular biology of fimbriae of enterotoxigenic Escherichia coli. Curr Top Microbiol Immunol. 1985;118:119–138. doi: 10.1007/978-3-642-70586-1_7. [DOI] [PubMed] [Google Scholar]
  25. Nuijten P. J., van Asten F. J., Gaastra W., van der Zeijst B. A. Structural and functional analysis of two Campylobacter jejuni flagellin genes. J Biol Chem. 1990 Oct 15;265(29):17798–17804. [PubMed] [Google Scholar]
  26. Ramirez R. M., Villarejo M. Osmotic signal transduction to proU is independent of DNA supercoiling in Escherichia coli. J Bacteriol. 1991 Jan;173(2):879–885. doi: 10.1128/jb.173.2.879-885.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rimsky S., Spassky A. Sequence determinants for H1 binding on Escherichia coli lac and gal promoters. Biochemistry. 1990 Apr 17;29(15):3765–3771. doi: 10.1021/bi00467a024. [DOI] [PubMed] [Google Scholar]
  28. Sack R. B. Human diarrheal disease caused by enterotoxigenic Escherichia coli. Annu Rev Microbiol. 1975;29:333–353. doi: 10.1146/annurev.mi.29.100175.002001. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Schmid M. B. More than just "histone-like" proteins. Cell. 1990 Nov 2;63(3):451–453. doi: 10.1016/0092-8674(90)90438-k. [DOI] [PubMed] [Google Scholar]
  31. Schneider K., Beck C. F. Promoter-probe vectors for the analysis of divergently arranged promoters. Gene. 1986;42(1):37–48. doi: 10.1016/0378-1119(86)90148-4. [DOI] [PubMed] [Google Scholar]
  32. Segers R. P., De Nijs A., van Kooten P. J., Gaastra W., van der Zeijst B. A. The use of immunodeficient male (CBA/N x BALB/c) F1 mice to produce monoclonal antibodies directed to proteins of Leptospira interrogans rather than to immunodominant lipopolysaccharides. Hybridoma. 1990 Jun;9(3):275–283. doi: 10.1089/hyb.1990.9.275. [DOI] [PubMed] [Google Scholar]
  33. Smith H. R., Willshaw G. A., Rowe B. Mapping of a plasmid, coding for colonization, factor antigen I and heat-stable enterotoxin production, isolated from an enterotoxigenic strain of Escherichia coli. J Bacteriol. 1982 Jan;149(1):264–275. doi: 10.1128/jb.149.1.264-275.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]

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