Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Dec;175(24):7976–7981. doi: 10.1128/jb.175.24.7976-7981.1993

Differential decay of RNA of the CFA/I fimbrial operon and control of relative gene expression.

B J Jordi 1, I E op den Camp 1, L A de Haan 1, B A van der Zeijst 1, W Gaastra 1
PMCID: PMC206977  PMID: 7504669

Abstract

CFA/I fimbriae on human enterotoxigenic Escherichia coli are composed of the CfaB protein, the product of the second gene of the CFA/I operon. We show here that CfaB is expressed at a higher level than other proteins of the CFA/I operon. mRNA encoding the CfaB protein is much more abundant than mRNA encoding CfaA, the first protein, together with CfaB or mRNA encoding CfaA only. Only one promoter, upstream of cfaA, is present. These data indicate that a primary transcript containing cfaA and cfaB is processed into a cfaA-specific mRNA and a cfaB-specific mRNA. The cfaA mRNA is unstable, while the cfaB mRNA is stable and therefore accumulates in CFA/I-producing E. coli. The cfaB mRNA is probably stabilized by a stem-loop structure downstream of the cfaB gene. No distinct mRNA fragments could be detected encoding the other two proteins, CfaC and CfaE, of the CFA/I operon. These results indicate that cfaC- and cfaE-specific mRNAs degrade very rapidly and/or are produced in small amounts.

Full text

PDF
7977

Images in this article

7978Image
on p.7978
7978Image
on p.7978
7979Image
on p.7979

Selected References

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

  1. Apirion D. Isolation, genetic mapping and some characterization of a mutation in Escherichia coli that affects the processing of ribonuleic acid. Genetics. 1978 Dec;90(4):659–671. doi: 10.1093/genetics/90.4.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belasco J. G., Higgins C. F. Mechanisms of mRNA decay in bacteria: a perspective. Gene. 1988 Dec 10;72(1-2):15–23. doi: 10.1016/0378-1119(88)90123-0. [DOI] [PubMed] [Google Scholar]
  3. Båga M., Göransson M., Normark S., Uhlin B. E. Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell. 1988 Jan 29;52(2):197–206. doi: 10.1016/0092-8674(88)90508-9. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chen C. Y., Beatty J. T., Cohen S. N., Belasco J. G. An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell. 1988 Feb 26;52(4):609–619. doi: 10.1016/0092-8674(88)90473-4. [DOI] [PubMed] [Google Scholar]
  6. Deutscher M. P. E. coli RNases: making sense of alphabet soup. Cell. 1985 Apr;40(4):731–732. doi: 10.1016/0092-8674(85)90330-7. [DOI] [PubMed] [Google Scholar]
  7. Donovan W. P., Kushner S. R. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1986 Jan;83(1):120–124. doi: 10.1073/pnas.83.1.120. [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. 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]
  11. 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]
  12. Jordi B. J., Dagberg B., de Haan L. A., Hamers A. M., van der Zeijst B. A., Gaastra W., Uhlin B. E. The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli. EMBO J. 1992 Jul;11(7):2627–2632. doi: 10.1002/j.1460-2075.1992.tb05328.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Karjalainen T. K., Evans D. G., Evans D. J., Jr, Graham D. Y., Lee C. H. Iron represses the expression of CFA/I fimbriae of enterotoxigenic E. coli. Microb Pathog. 1991 Nov;11(5):317–323. doi: 10.1016/0882-4010(91)90017-5. [DOI] [PubMed] [Google Scholar]
  16. Kirsebom L. A., Baer M. F., Altman S. Differential effects of mutations in the protein and RNA moieties of RNase P on the efficiency of suppression by various tRNA suppressors. J Mol Biol. 1988 Dec 20;204(4):879–888. doi: 10.1016/0022-2836(88)90048-4. [DOI] [PubMed] [Google Scholar]
  17. Krogfelt K. A. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli. Rev Infect Dis. 1991 Jul-Aug;13(4):721–735. doi: 10.1093/clinids/13.4.721. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lundberg U., von Gabain A., Melefors O. Cleavages in the 5' region of the ompA and bla mRNA control stability: studies with an E. coli mutant altering mRNA stability and a novel endoribonuclease. EMBO J. 1990 Sep;9(9):2731–2741. doi: 10.1002/j.1460-2075.1990.tb07460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Newbury S. F., Smith N. H., Higgins C. F. Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell. 1987 Dec 24;51(6):1131–1143. doi: 10.1016/0092-8674(87)90599-x. [DOI] [PubMed] [Google Scholar]
  21. Nilsson P., Uhlin B. E. Differential decay of a polycistronic Escherichia coli transcript is initiated by RNaseE-dependent endonucleolytic processing. Mol Microbiol. 1991 Jul;5(7):1791–1799. doi: 10.1111/j.1365-2958.1991.tb01928.x. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. Srivastava S. K., Cannistraro V. J., Kennell D. Broad-specificity endoribonucleases and mRNA degradation in Escherichia coli. J Bacteriol. 1992 Jan;174(1):56–62. doi: 10.1128/jb.174.1.56-62.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Studier F. W. Genetic mapping of a mutation that causes ribonucleases III deficiency in Escherichia coli. J Bacteriol. 1975 Oct;124(1):307–316. doi: 10.1128/jb.124.1.307-316.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES