1887

Abstract

During the last few years, several genes, such as , and , have been shown to be coregulated by the histone-like nucleoid-structuring (H-NS) protein and the cyclic AMP-catabolite activator protein (cAMP/CAP) complex, suggesting an interaction between both systems in the control of some cellular functions. In this study, the possible effect of H-NS on the cAMP level was investigated. In a CAP-deficient strain, the presence of an mutation results in a strong reduction in the amount of cAMP, due to a decrease in adenylate cyclase activity. This is caused by the reduced expression of , which encodes the Enzyme IIA of the phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS), from its specific P2 promoter. This leads to a twofold reduction in the global amount of Enzyme IIA, the adenylate cyclase activator, responsible for the decrease in adenylate cyclase activity observed in the strain.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-5-1553
2002-05-01
2024-11-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/5/1481553a.html?itemId=/content/journal/micro/10.1099/00221287-148-5-1553&mimeType=html&fmt=ahah

References

  1. Aiba H. 1985; Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J Biol Chem 260:3063–3070
    [Google Scholar]
  2. Atlung T., Ingmer H. 1997; H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24:7–17 [CrossRef]
    [Google Scholar]
  3. Balsalobre C., Johansson J., Uhlin B. E., Juarez A., Munoa F. J. 1999; Alterations in protein expression caused by the hha mutation in Escherichia coli : influence of growth medium osmolarity. J Bacteriol 181:3018–3024
    [Google Scholar]
  4. Bertin P., Terao E., Lee E. H., Lejeune P., Colson C., Danchin A., Collatz E. 1994; The H-NS protein is involved in the biogenesis of flagella in Escherichia coli . J Bacteriol 176:5537–5540
    [Google Scholar]
  5. Bertin P., Hommais F., Krin E., Soutourina O., Tendeng C., Derzelle S., Danchin A. 2001; H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie 83:235–241 [CrossRef]
    [Google Scholar]
  6. Busby S., Kolb A. 1996; The CAP modulon. In Regulation of Gene Expression in Escherichia coli pp 255–279 Edited by Lin E. C. C. Lynch A. S. Austin, TX: R. G. Landes;
    [Google Scholar]
  7. Calvo J. M., Matthews R. 1994; The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli . Microbiol Rev 58:466–490
    [Google Scholar]
  8. Coll J. L., Heyde M., Portalier R. 1994; Expression of the nmpC gene of Escherichia coli K-12 is modulated by external pH. Identification of cis -acting regulatory sequences involved in this regulation. Mol Microbiol 12:83–93 [CrossRef]
    [Google Scholar]
  9. Crasnier M., Danchin A. 1990; Characterization of Escherichia coli adenylate cyclase mutants with modified regulation. J Gen Microbiol 136:1825–1831 [CrossRef]
    [Google Scholar]
  10. Crasnier M., Dumay V., Danchin A. 1994; The catalytic domain of Escherichia coli K-12 adenylate cyclase as revealed by deletion analysis of the cya gene. Mol Gen Genet 243:409–416 [CrossRef]
    [Google Scholar]
  11. Crasnier-Mednansky M., Park M. C., Studley W. K., Saier M. H. Jr 1997; Cra-mediated regulation of Escherichia coli adenylate cyclase. Microbiology 143:785–792 [CrossRef]
    [Google Scholar]
  12. Den Blaauwen J. L., Postma P. W. 1985; Regulation of cyclic AMP synthesis by enzyme IIIGlc of the phosphoenolpyruvate: sugar phosphotransferase system in crp strains of Salmonella typhimurium . J Bacteriol 164:477–478
    [Google Scholar]
  13. De Reuse H., Danchin A. 1988; The ptsH , ptsI , and crr genes of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system: a complex operon with several modes of transcription. J Bacteriol 170:3827–3837
    [Google Scholar]
  14. De Reuse H., Touati E., Glaser P., Danchin A. 1986; Low copy number plasmid vectors for gene cloning and for monitoring gene expression. FEMS Microbiol Lett 37:193–197 [CrossRef]
    [Google Scholar]
  15. De Reuse H., Kolb A., Danchin A. 1992; Positive regulation of the expression of the Escherichia coli pts operon. Identification of the regulatory regions. J Mol Biol 226:623–635 [CrossRef]
    [Google Scholar]
  16. Forsman K., Uhlin B. E., Sondén B., Göransson M. 1992; Antirepression function in Escherichia coli for the cAMP–cAMP receptor protein transcriptional activator. Proc Natl Acad Sci USA 89:9880–9884 [CrossRef]
    [Google Scholar]
  17. Gonzalez-Pastor J. E., San Millan J. L., Castilla M. A., Moreno F. 1995; Structure and organization of plasmid genes required to produce the translation inhibitor microcin C7. J Bacteriol 177:7131–7140
    [Google Scholar]
  18. Guidi-Rontani C., Danchin A., Ullmann A. 1981; Isolation and characterization of an Escherichia coli mutant affected in the regulation of adenylate cyclase. J Bacteriol 148:753–761
    [Google Scholar]
  19. Hommais F., Krin E., Laurent-Winter C., Soutourina O., Malpertuy A., Le Caer J. P., Danchin A., Bertin P. 2001; Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40:20–36 [CrossRef]
    [Google Scholar]
  20. Inada T., Takahashi H., Mizuno T., Aiba H. 1996; Down regulation of cAMP production by cAMP receptor protein in Escherichia coli : an assessment of the contributions of transcriptional and posttranscriptional control of adenylate cyclase. Mol Gen Genet 253:198–204 [CrossRef]
    [Google Scholar]
  21. Johansson J., Dagberg B., Richet E., Uhlin B. E. 1998; H-NS and StpA proteins stimulate expression of the maltose regulon in Escherichia coli . J Bacteriol 180:6117–6125
    [Google Scholar]
  22. Joseph E., Bernsley C., Guiso N., Ullmann A. 1982; Multiple regulation of the activity of adenylate cyclase in Escherichia coli . Mol Gen Genet 185:262–268 [CrossRef]
    [Google Scholar]
  23. Kawamukai M., Kishimoto J., Utsumi R., Himeno M., Komano T., Aiba H. 1985; Negative regulation of adenylate cyclase gene ( cya) expression by cyclic AMP–cyclic AMP receptor protein in Escherichia coli : studies with cya - lac protein and operon fusion plasmids. J Bacteriol 164:872–877
    [Google Scholar]
  24. Kolb A., Busby S., Buc H., Garges S., Adhya S. 1993; Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62:749–795 [CrossRef]
    [Google Scholar]
  25. Laurent-Winter C., Ngo S., Danchin A., Bertin P. 1997; Role of Escherichia coli histone-like nucleoid structuring protein in bacterial metabolism and stress response: identification of targets by two-dimensional electrophoresis. Eur J Biochem 244:767–773 [CrossRef]
    [Google Scholar]
  26. Levinthal M., Lejeune P., Danchin A. 1994; The H-NS protein modulates the activation of the ilvIH operon of Escherichia coli K12 by Lrp, the leucine regulatory protein. Mol Gen Genet 242:736–743
    [Google Scholar]
  27. Levy S., Zeng G.-Q., Danchin A. 1990; Cyclic AMP synthesis in Escherichia coli strains bearing known deletions in the pts phosphotransferase operon. Gene 86:27–33 [CrossRef]
    [Google Scholar]
  28. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Miller J. H. 1992 A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Mitchell W. J., Saffen D. W., Roseman S. 1987; Sugar transport by the bacterial phosphotransferase system: in vivo regulation of lactose transport in Escherichia coli by IIIGlc, a protein of the phosphoenolpyruvate: glucose phosphotransferase system. J Biol Chem 262:16254–16260
    [Google Scholar]
  31. Nieto J. M., Madrid C., Prenafeta A., Miquelay E., Balsalobre C., Carrascal M., Juarez A. 2000; Expression of the hemolysin operon in Escherichia coli is modulated by a nucleoid-protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263:349–358 [CrossRef]
    [Google Scholar]
  32. Oshima T., Ito K., Kabayama H., Nakamura Y. 1995; Regulation of lrp gene expression by H-NS and Lrp proteins in Escherichia coli : dominant negative mutations in lrp . Mol Gen Genet 247:521–528 [CrossRef]
    [Google Scholar]
  33. Peterkofsky A., Seok Y.-J., Amin N. 8 other authors 1995; The Escherichia coli adenylyl cyclase complex: requirement of PTS proteins for stimulation by nucleotides. Biochem 34:8950–8959 [CrossRef]
    [Google Scholar]
  34. Postma P. W., Lengeler J. W. 1985; Phosphoenolpyruvate: carbohydrate phosphotransferase system of bacteria. Microbiol Rev 49:232–269
    [Google Scholar]
  35. Potter K., Chaloner-Larsson G., Yamazaki H. 1974; Abnormally high rate of cyclic AMP excretion from an Escherichia coli mutant deficient in cyclic AMP receptor protein. Biochem Biophys Res Commun 57:379–385 [CrossRef]
    [Google Scholar]
  36. Reddy P., Kamireddi M. 1998; Modulation of Escherichia coli adenylyl cyclase activity by catalytic-site mutants of protein IIAGlc of the phosphoenolpyruvate: sugar phosphotransferase system. J Bacteriol 180:732–736
    [Google Scholar]
  37. Rephaeli A. W., Saier M. H. Jr 1976; Effects of crp mutations on adenosine 3′,5′-monophosphate metabolism in Salmonella typhimurium . J Bacteriol 127:120–127
    [Google Scholar]
  38. Roy A., Haziza C., Danchin A. 1983; Regulation of adenylate cyclase synthesis in Escherichia coli : nucleotide sequence of the control region. EMBO J 2:791–797
    [Google Scholar]
  39. Roy A., Glaser P., Danchin A. 1988; Aspects of the regulation of adenylate cyclase synthesis in Escherichia coli K12. J Gen Microbiol 134:359–367
    [Google Scholar]
  40. Ryu S., Garges S. 1994; Promoter switch in the Escherichia coli pts operon. J Biol Chem 269:4767–4772
    [Google Scholar]
  41. Ryu S., Ramseier T. M., Michotey V., Garges S., Saier M. H. Jr 1995; Effect of the FruR regulator on transcription of the pts operon in Escherichia coli . J Biol Chem 270:2489–2496 [CrossRef]
    [Google Scholar]
  42. Saier M. H. Jr, Ramseier T. M., Reizer J. others 1996; Regulation of carbon utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology . pp 1325–1343 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
  43. Schnetz K., Wang J. C. 1996; Silencing of the Escherichia coli bgl promoter: effects of template supercoiling and cell extracts on promoter activity in vitro . Nucleic Acids Res 24:2422–2428 [CrossRef]
    [Google Scholar]
  44. Soutourina O., Kolb A., Krin E., Laurent-Winter C., Rimsky S., Danchin A., Bertin P. 1999; Multiple control of flagellum biosynthesis in Escherichia coli : role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181:7500–7508
    [Google Scholar]
  45. Takahashi H., Inada T., Postma P., Aiba H. 1998; CRP down-regulates adenylate cyclase activity by reducing the level of phosphorylated IIAGlc, the glucose-specific phosphotransferase protein, in Escherichia coli . Mol Gen Genet 259:317–326 [CrossRef]
    [Google Scholar]
  46. Tanaka Y., Kimata K., Inada T., Tagami H., Aiba H. 1999; Negative regulation of the pts operon by Mlc: mechanism underlying glucose induction in Escherichia coli . Genes Cells 4:391–399 [CrossRef]
    [Google Scholar]
  47. Yang J. K., Epstein W. 1983; Purification and characterization of adenylate cyclase from Escherichia coli K12. J Biol Chem 258:3750–3758
    [Google Scholar]
  48. Zeng G. Q., De Reuse H., Danchin A. 1992; Mutational analysis of the enzyme IIIGlc of the phosphoenolpyruvate phosphotransferase system in Escherichia coli . Res Microbiol 143:251–261 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/00221287-148-5-1553
Loading
/content/journal/micro/10.1099/00221287-148-5-1553
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error