1887

Abstract

The promoter (P) regulates transcription of two genes, and , that are required for the synthesis of guanosine 5′-monophosphate (GMP), a precursor for the synthesis of guanine nucleoside triphosphates. Transcription from P increases as a function of increasing cellular growth rate, and this is referred to as growth rate-dependent control (GRDC). Here we investigated the role of the factor for inversion stimulation (FIS) in the regulation of this promoter. The results showed that there are three binding sites for FIS centred near positions −11, +8 and +29 relative to the transcription start site. Binding of FIS to these sites results in repression of P but not . Deletion of the gene results in increased P activity , but GRDC of P is maintained.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/016774-0
2008-06-01
2024-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/6/1729.html?itemId=/content/journal/micro/10.1099/mic.0.2008/016774-0&mimeType=html&fmt=ahah

References

  1. Aiyar S. E., McLeod S. M., Ross W., Hirvonen C. A., Thomas M. S., Johnson R. C., Gourse R. L. 2002; Architecture of Fis-activated transcription complexes at the Escherichia coli rrnB P1 and rrnE P1 promoters. J Mol Biol 316:501–516
    [Google Scholar]
  2. Ali Azam T., Iwata A., Nishimura A., Ueda S., Ishihama A. 1999; Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181:6361–6370
    [Google Scholar]
  3. Appleman J. A., Ross W., Salomon J., Gourse R. L. 1998; Activation of Escherichia coli rRNA transcription by FIS during a growth cycle. J Bacteriol 180:1525–1532
    [Google Scholar]
  4. Ball C. A., Osuna R., Ferguson K. C., Johnson R. C. 1992; Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli . J Bacteriol 174:8043–8056
    [Google Scholar]
  5. Bokal A. J., Ross W., Gourse R. L. 1995; The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. J Mol Biol 245:197–207
    [Google Scholar]
  6. Bradley M. D., Beach M. B., de Koning A. P., Pratt T. S., Osuna R. 2007; Effects of FIS on Escherichia coli gene expression during different growth stages. Microbiology 153:2922–2940
    [Google Scholar]
  7. Browning D. F., Cole J. A., Busby S. J. 2000; Suppression of FNR-dependent transcription activation at the Escherichia coli nir promoter by Fis, IHF and H-NS: modulation of transcription initiation by a complex nucleo-protein assembly. Mol Microbiol 37:1258–1269
    [Google Scholar]
  8. Browning D. F., Beatty C. M., Sanstad E. A., Gunn K. E., Busby S. J. W., Wolfe A. J. 2004; Modulation of CRP-dependent transcription at the Escherichia coli acsP2 promoter by nucleoprotein complexes: anti-activation by the nucleoid proteins FIS and IHF. Mol Microbiol 51:241–254
    [Google Scholar]
  9. Claret L., Rouviere-Yaniv J. 1996; Regulation of HU alpha and HU beta by CRP and FIS in Escherichia coli . J Mol Biol 263:126–139
    [Google Scholar]
  10. Davies I. J., Drabble W. T. 1996; Stringent and growth-rate-dependent control of the gua operon of Escherichia coli K-12. Microbiology 142:2429–2437
    [Google Scholar]
  11. Dennis P. P., Ehrenberg M., Bremer H. 2004; Control of rRNA synthesis in Escherichia coli : a systems biology approach. Microbiol Mol Biol Rev 68:639–668
    [Google Scholar]
  12. Dong H., Kirsebom L. A., Nilsson L. 1996; Growth rate regulation of 4.5 S RNA and M1 RNA the catalytic subunit of Escherichia coli RNase P. J Mol Biol 261:303–308
    [Google Scholar]
  13. Emilsson V., Nilsson L. 1995; Factor for inversion stimulation-dependent growth rate regulation of serine and threonine tRNA species. J Biol Chem 270:16610–16614
    [Google Scholar]
  14. Estrem S. T., Gaal T., Ross W., Gourse R. L. 1998; Identification of an UP element consensus sequence for bacterial promoters. Proc Natl Acad Sci U S A 95:9761–9766
    [Google Scholar]
  15. Falconi M., Brandi A., La Teana A., Gualerzi C. O., Pon C. L. 1996; Antagonistic involvement of FIS and H-NS proteins in the transcriptional control of hns expression. Mol Microbiol 19:965–975
    [Google Scholar]
  16. Finkel S. E., Johnson R. C. 1992; The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol 6:3257–3265
    [Google Scholar]
  17. Gonzalez-Gil G., Kahmann R., Muskhelishvili G. 1998; Regulation of crp transcription by oscillation between distinct nucleoprotein complexes. EMBO J 17:2877–2885
    [Google Scholar]
  18. Gourse R. L., Gaal T., Bartlett M. S., Appleman J. A., Ross W. 1996; rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli . Annu Rev Microbiol 50:645–677
    [Google Scholar]
  19. Grainger D. C., Hurd D., Goldberg M. D., Busby S. J. W. 2006; Association of nucleiod proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34:4642–4652
    [Google Scholar]
  20. Hengen P. N., Bartram S. L., Stewart L. E., Schneider T. D. 1997; Information analysis of Fis binding sites. Nucleic Acids Res 25:4994–5002
    [Google Scholar]
  21. Husnain S. I., Thomas M. S. 2008; The UP element is necessary but not sufficient for growth rate-dependent control of the Escherichia coli guaB promoter. J Bacteriol 190:2450–2457
    [Google Scholar]
  22. Hutchings M. I., Drabble W. T. 2000; Regulation of the divergent guaBA and xseA promoters of Escherichia coli by the cyclic AMP receptor protein. FEMS Microbiol Lett 187:115–122
    [Google Scholar]
  23. Jackson L., Blake T., Green J. 2004; Regulation of ndh expression in Escherichia coli by Fis. Microbiology 150:407–413
    [Google Scholar]
  24. Lazarus L. R., Travers A. A. 1993; The Escherichia coli FIS protein is not required for the activation of tyrT transcription on entry into exponential growth. EMBO J 12:2483–2494
    [Google Scholar]
  25. Mallik P., Paul B. J., Rutherford S. T., Gourse R. L., Osuna R. 2006; DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli . J Bacteriol 188:5775–5782
    [Google Scholar]
  26. McLeod S. M., Aiyar S. E., Gourse R. L., Johnson R. C. 2002; The C-terminal domains of the RNA polymerase α subunits: contact site with Fis and localization during co-activation with CRP at the Escherichia coli proP P2 promoter. J Mol Biol 316:517–529
    [Google Scholar]
  27. Mehra R. K., Drabble W. T. 1981; Dual control of the gua operon of Escherichia coli K12 by adenine and guanine nucleotides. J Gen Microbiol 123:27–37
    [Google Scholar]
  28. Meng L. M., Kilstrup M., Nygaard P. 1990; Autoregulation of PurR repressor synthesis and involvement of purR in the regulation of purB, purC, purL, purMN and guaBA expression in Escherichia coli . Eur J Biochem 187:373–379
    [Google Scholar]
  29. Meng W., Savery N. J., Busby S. J. W., Thomas M. S. 2000; The Escherichia coli RNA polymerase α subunit linker: length requirements for transcription activation at CRP-dependent promoters. EMBO J 19:1555–1566
    [Google Scholar]
  30. Meng W., Belyaeva T., Savery N. J., Busby S. J., Ross W. E., Gaal T., Gourse R. L., Thomas M. S. 2001; UP element-dependent transcription at the Escherichia coli rrnB P1 promoter: positional requirements and role of the RNA polymerase alpha subunit linker. Nucleic Acids Res 29:4166–4178
    [Google Scholar]
  31. Miller J. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  32. Newlands J. T., Ross W., Gosink K. K., Gourse R. L. 1991; Factor-independent activation of Escherichia coli rRNA transcription. II. characterization of complexes of rrnB P1 promoters containing or lacking the upstream activator region with Escherichia coli RNA polymerase. J Mol Biol 220:569–583
    [Google Scholar]
  33. Nilsson L., Verbeek H., Vijgenboom E., van-Drunen C., Vanet A., Bosch L. 1992; FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol 174:921–929
    [Google Scholar]
  34. Paul B. J., Ross W., Gaal T., Gourse R. L. 2004; rRNA transcription in Escherichia coli . Annu Rev Genet 38:749–770
    [Google Scholar]
  35. Pemberton I. K., Muskhelishvili G., Travers A. A., Buckle M. 2002; FIS modulates the kinetics of successive interactions of RNA polymerase with the core and upstream regions of the tyrT promoter. J Mol Biol 318:651–663
    [Google Scholar]
  36. Quandt K., Frech K., Karas H., Wingender E., Werner T. 1995; MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23:4878–4884
    [Google Scholar]
  37. Rao L., Ross W., Appleman J. A., Gaal T., Leirmo S., Schlax P. J., Record M. T. Jr, Gourse R. L. 1994; Factor independent activation of rrnB P1. An “extended” promoter with an upstream element that dramatically increases promoter strength. J Mol Biol 235:1421–1435
    [Google Scholar]
  38. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. 1990; Escherichia coli Fis protein activates ribosomal RNA transcription in vitro and in vivo . EMBO J 9:3733–3742
    [Google Scholar]
  39. Ross W., Aiyar S. E., Salomon J., Gourse R. L. 1998; Escherichia coli promoters with UP elements of different strengths: modular structure of bacterial promoters. J Bacteriol 180:5375–5383
    [Google Scholar]
  40. Ross W., Salomon J., Holmes W. M., Gourse R. L. 1999; Activation of Escherichia coli leuV transcription by FIS. J Bacteriol 181:3864–3868
    [Google Scholar]
  41. Schneider R., Travers A., Muskhelishvili G. 1997; FIS modulates growth phase-dependent topological transitions of DNA in Escherichia coli . Mol Microbiol 26:519–530
    [Google Scholar]
  42. Shao Y., Feldman-Cohen L. S., Osuna R. 2008; Functional characterisation of the Escherichia coli Fis-DNA binding sequence. J Mol Biol 376:771–785
    [Google Scholar]
  43. Shultzaberger R. K., Roberts L. R., Lyakhov I. G., Sidorov I. A., Stephen A. G., Fisher R. J., Schneider T. D. 2007; Correlation between binding rate constants and individual information of E. coli Fis binding sites. Nucleic Acids Res 35:5275–5283
    [Google Scholar]
  44. Simons R. W., Houman F., Kleckner N. 1987; Improved single and multicopy lac -based cloning vectors for protein and operon fusions. Gene 53:85–96
    [Google Scholar]
  45. Tesfa-Selase F., Drabble W. T. 1996; Specific binding of DnaA protein to a DnaA box in the guaB gene of Escherichia coli K12. Eur J Biochem 241:411–416
    [Google Scholar]
  46. Tiedeman A. A., Smith J. M. 1984; Isolation and characterization of regulatory mutations affecting the expression of the guaBA operon of Escherichia coli K-12. Mol Gen Genet 195:77–82
    [Google Scholar]
  47. Travers A., Schneider R., Muskhelishvili G. 2001; DNA supercoiling and transcription in Escherichia coli : the FIS connection. Biochimie 83:213–217
    [Google Scholar]
  48. Weinstein-Fischer D., Elgrably-Weiss M., Altuvia S. 2000; Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413–1420
    [Google Scholar]
  49. Wu H., Tyson K. L., Cole J. A., Busby S. J. W. 1998; Regulation of transcription initiation at the Escherichia coli nir operon promoter: a new mechanism to account for co-dependence on two transcription factors. Mol Microbiol 27:493–505
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.2008/016774-0
Loading
/content/journal/micro/10.1099/mic.0.2008/016774-0
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