1887

Abstract

The cellular level of the heat-shock sigma factor RpoH ( ) is negatively controlled by chaperone-mediated proteolysis through the essential metalloprotease FtsH. Point mutations in the highly conserved region 2.1 stabilize RpoH . To assess the importance of this turnover element, hybrid proteins were constructed between RpoH and RpoH, a stable RpoH protein that differs from region 2.1 of RpoH at several positions. Nine amino acids forming a putative -helix were exchanged between the two proteins. Both hybrids were active sigma factors and showed intermediate protein stability. Introduction of RpoH region 2.1 into the general stress sigma factor RpoS, which is a substrate of the ClpXP protease, did not render RpoS susceptible to FtsH. Hence, region 2.1 alone is not sufficient to confer FtsH sensitivity to other proteins. Region 2.1 is not a major chaperone-binding site since DnaK and DnaJ bound efficiently to all RpoH variants. The stability of the mutated RpoH proteins correlated with their stability in a purified degradation system, suggesting that region 2.1 might be directly involved in the interaction with the FtsH protease.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/007047-0
2007-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2560.html?itemId=/content/journal/micro/10.1099/mic.0.2007/007047-0&mimeType=html&fmt=ahah

References

  1. Arsène F., Tomoyasu T., Mogk A., Schirra C., Schulze-Specking A., Bukau B. 1999; Role of region C in regulation of the heat shock gene-specific sigma factor of Escherichia coli , σ 32 . J Bacteriol 181:3552–3561
    [Google Scholar]
  2. Becker G., Klauck E., Hengge-Aronis R. 1999; Regulation of RpoS proteolysis in Escherichia coli : the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci U S A 96:6439–6444
    [Google Scholar]
  3. Bertani D., Oppenheim A. B., Narberhaus F. 2001; An internal region of the RpoH heat shock transcription factor is critical for rapid degradation by the FtsH protease. FEBS Lett 493:17–20
    [Google Scholar]
  4. Blaszczak A., Georgopoulos C., Liberek K. 1999; On the mechanism of FtsH-dependent degradation of the σ 32 transcriptional regulator of Escherichia coli and the role of the DnaK chaperone machine. Mol Microbiol 31:157–166
    [Google Scholar]
  5. Campbell E. A., Tupy J. L., Gruber T. M., Wang S., Sharp M. M., Gross C. A., Darst S. A. 2003; Crystal structure of Escherichia coli σ E with the cytoplasmic domain of its anti-sigma RseA. Mol Cell 11:1067–1078
    [Google Scholar]
  6. Dartigalongue C., Loferer H., Raina S. 2001; EcfE, a new essential inner membrane protease: its role in the regulation of heat shock response in Escherichia coli . EMBO J 20:5908–5918
    [Google Scholar]
  7. Dautin N., Karimova G., Ullmann A., Ladant D. 2000; Sensitive genetic screen for protease activity based on a cyclic AMP signaling cascade in Escherichia coli . J Bacteriol 182:7060–7066
    [Google Scholar]
  8. El-Samad H., Kurata H., Doyle J. C., Gross C. A., Khammash M. 2005; Surviving heat shock: control strategies for robustness and performance. Proc Natl Acad Sci U S A 102:2736–2741
    [Google Scholar]
  9. Führer F., Langklotz S., Narberhaus F. 2006; The C-terminal end of LpxC is required for degradation by the FtsH protease. Mol Microbiol 59:1025–1036
    [Google Scholar]
  10. Gamer J., Multhaup G., Tomoyasu T., McCarty J. S., Rüdiger S., Schönfeld H. J., Schirra C., Bujard H., Bukau B. 1996; A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor σ 32 . EMBO J 15:607–617
    [Google Scholar]
  11. Germer J., Becker G., Metzner M., Hengge-Aronis R. 2001; Role of activator site position and a distal UP-element half-site for sigma factor selectivity at a CRP/H-NS-activated σ s-dependent promoter in Escherichia coli . Mol Microbiol 41:705–716
    [Google Scholar]
  12. Gottesman S. 1999; Regulation by proteolysis: developmental switches. Curr Opin Microbiol 2:142–147
    [Google Scholar]
  13. Gross C. A. others 1996; Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology . pp 1382–1399 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
  14. Gruber T. M., Gross C. A. 2003; Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466
    [Google Scholar]
  15. Guisbert E., Herman C., Lu C. Z., Gross C. A. 2004; A chaperone network controls the heat shock response in E. coli . Genes Dev 18:2812–2821
    [Google Scholar]
  16. Hengge R., Bukau B. 2003; Proteolysis in prokaryotes: protein quality control and regulatory principles. Mol Microbiol 49:1451–1462
    [Google Scholar]
  17. Herman C., Thévenet D., D'Ari R., Bouloc P. 1995; Degradation of σ 32, the heat shock regulator in Escherichia coli , is governed by HflB. Proc Natl Acad Sci U S A 92:3516–3520
    [Google Scholar]
  18. Herman C., Thévenet D., D'Ari R., Bouloc P. 1997; The HflB protease of Escherichia coli degrades its inhibitor λ cIII. J Bacteriol 179:358–363
    [Google Scholar]
  19. Herman C., Prakash S., Lu C. Z., Matouschek A., Gross C. A. 2003; Lack of a robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Mol Cell 11:659–669
    [Google Scholar]
  20. Holt C., Sawyer L. 1988; Primary and predicted secondary structures of the caseins in relation to their biological functions. Protein Eng 2:251–259
    [Google Scholar]
  21. Horikoshi M., Yura T., Tsuchimoto S., Fukumori Y., Kanemori M. 2004; Conserved region 2.1 of Escherichia coli heat shock transcription factor σ 32 is required for modulating both metabolic stability and transcriptional activity. J Bacteriol 186:7474–7480
    [Google Scholar]
  22. Ito K., Akiyama Y. 2005; Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231
    [Google Scholar]
  23. Jenal U., Hengge-Aronis R. 2003; Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6:163–172
    [Google Scholar]
  24. Kihara A., Akiyama Y., Ito K. 1997; Host regulation of lysogeny decision in bacteriophage λ : transmembrane modulation of FtsH (HflB), the cII degrading protease, by HflKC (HflA. Proc Natl Acad Sci U S A 94:5544–5549
    [Google Scholar]
  25. Lange R., Hengge-Aronis R. 1994; The cellular concentration of the σ S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev 8:1600–1612
    [Google Scholar]
  26. Leffers G. G. Jr, Gottesman S. 1998; Lambda Xis degradation in vivo by Lon and FtsH. J Bacteriol 180:1573–1577
    [Google Scholar]
  27. Liberek K., Galitzki T. P., Zylicz M., Georgopoulos C. 1992; The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the σ 32 transcription factor. Proc Natl Acad Sci U S A 89:3516–3520
    [Google Scholar]
  28. Lonetto M., Gribskov M., Gross C. A. 1992; The σ 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849
    [Google Scholar]
  29. McCarty J. S., Rüdiger S., Schönfeld H. J., Schneider-Mergener J., Nakahigashi K, Yura T., Bukau B. 1996; Regulatory region C of the E. coli heat shock transcription factor, σ 32, constitutes a DnaK binding site and is conserved among eubacteria. J Mol Biol 256:829–837
    [Google Scholar]
  30. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
  31. Murakami K. S., Masuda S., Darst S. A. 2002; Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Å resolution. Science 296:1280–1284
    [Google Scholar]
  32. Nagai H., Yuzawa H., Kanemori M., Yura T. 1994; A distinct segment of the σ 32 polypeptide is involved in DnaK-mediated negative control of the heat shock response in Escherichia coli . Proc Natl Acad Sci U S A 91:10280–10284
    [Google Scholar]
  33. Narberhaus F., Balsiger S. 2003; Structure-function studies of Escherichia coli RpoH ( σ 32) by in vitro linker insertion mutagenesis. J Bacteriol 185:2731–2738
    [Google Scholar]
  34. Narberhaus F., Weiglhofer W., Fischer H. M., Hennecke H. 1996; The Bradyrhizobium japonicum rpoH 1 gene encoding a σ 32-like protein is part of a unique heat shock gene cluster together with groESL 1 and three small heat shock genes. J Bacteriol 178:5337–5346
    [Google Scholar]
  35. Narberhaus F., Krummenacher P., Fischer H. M., Hennecke H. 1997; Three disparately regulated genes for σ 32-like transcription factors in Bradyrhizobium japonicum . Mol Microbiol 24:93–104
    [Google Scholar]
  36. Narberhaus F., Kowarik M., Beck C., Hennecke H. 1998; Promoter selectivity of the Bradyrhizobium japonicum RpoH transcription factors in vivo and in vitro. J Bacteriol 180:2395–2401
    [Google Scholar]
  37. Obrist M., Narberhaus F. 2005; Identification of a turnover element in region 2.1 of Escherichia coli σ 32 by a bacterial one-hybrid approach. J Bacteriol 187:3807–3813
    [Google Scholar]
  38. Ogura T., Inoue K., Tatsuta T., Suzaki T., Karata K., Young K., Su L. H., Fierke C. A., Jackman J. E. other authors 1999; Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli . Mol Microbiol 31:833–844
    [Google Scholar]
  39. Rist W., Jorgensen T. J., Roepstorff P., Bukau B., Mayer M. P. 2003; Mapping temperature-induced conformational changes in the Escherichia coli heat shock transcription factor σ 32 by amide hydrogen exchange. J Biol Chem 278:51415–51421
    [Google Scholar]
  40. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor; New York: Cold Spring Harbor Laboratory Press;
  41. Shotland Y., Koby S., Teff D., Mansur N., Oren D. A., Tatematsu K., Tomoyasu T., Kessel M., Bukau B. other authors 1997; Proteolysis of the phage l CII regulatory protein by FtsH (HflB) of Escherichia coli . Mol Microbiol 24:1303–1310
    [Google Scholar]
  42. Shotland Y., Shifrin A., Ziv T., Teff D., Koby S., Kobiler O., Oppenheim A. B. 2000a; Proteolysis of bacteriophage λ CII by Escherichia coli FtsH (HflB. J Bacteriol 182:3111–3116
    [Google Scholar]
  43. Shotland Y., Teff D., Koby S., Kobiler O., Oppenheim A. B. 2000b; Characterization of a conserved α -helical, coiled-coil motif at the C-terminal domain of the ATP-dependent FtsH (HflB) protease of Escherichia coli . J Mol Biol 299:953–964
    [Google Scholar]
  44. Straus D., Walter W., Gross C. A. 1990; DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of σ 32 . Genes Dev 4:2202–2209
    [Google Scholar]
  45. Stüdemann A., Noirclerc-Savoye M., Klauck E., Becker G., Schneider D., Hengge R. 2003; Sequential recognition of two distinct sites in σ S by the proteolytic targeting factor RssB and ClpX. EMBO J 22:4111–4120
    [Google Scholar]
  46. Studier F. W., Moffatt B. A. 1986; Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189:113–130
    [Google Scholar]
  47. Tatsuta T., Tomoyasu T., Bukau B., Kitagawa M., Mori H., Karata K., Ogura T. 1998; Heat shock regulation in the ftsH null mutant of Escherichia coli : dissection of stability and activity control mechanisms of σ 32 in vivo . Mol Microbiol 30:583–593
    [Google Scholar]
  48. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
    [Google Scholar]
  49. Tomoyasu T., Gamer J., Bukau B., Kanemori M., Mori H., Rutman A. J., Oppenheim A. B., Yura T., Yamanaka K., Niki H. other authors 1995; Escherichia coli FtsH is a membrane bound, ATP-dependent protease which degrades the heat-shock transcription factor σ 32 . EMBO J 14:2551–2560
    [Google Scholar]
  50. Urech C., Koby S., Oppenheim A. B., Münchbach M., Hennecke H., Narberhaus F. 2000; Differential degradation of Escherichia coli σ 32 and Bradyrhizobium japonicum RpoH factors by the FtsH protease. Eur J Biochem 267:4831–4839
    [Google Scholar]
  51. Vassylyev D. G., Sekine S., Laptenko O., Lee J., Vassylyeva M. N., Borukhov S., Yokoyama S. 2002; Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature 417:712–719
    [Google Scholar]
  52. Yura T., Kanemori M., Morita M. T. 2000; The heat shock response: regulation and function. In Bacterial Stress Responses pp 3–18 Edited by Storz G., Hengge-Aronis R. Washington, DC: ASM Press;
    [Google Scholar]
  53. Zhou Y. N., Kusukawa N., Erickson J. W., Gross C. A., Yura T. 1988; Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor σ 32 . J Bacteriol 170:3640–3649
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/007047-0
Loading
/content/journal/micro/10.1099/mic.0.2007/007047-0
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