1887

Abstract

In , is the last gene of the operon. It encodes the repressor HspR, which regulates the expression from this operon by binding to a consensus upstream sequence known as HAIR (spR-ssociated nverted epeats). Previous investigations in the related Gram-positive bacterium have revealed that DnaK acts as a co-repressor for HspR. In this investigation, a similar situation was encountered using the corresponding mycobacterial pair. However, the novel feature unearthed in this study is that the mycobacterial GroELs, GroEL1 and GroEL2, considerably stimulate the HAIR-binding activity of the HspR-DnaK combination. That these GroELs play a role in the folding process was evident from the observation that when heat- or chemically denatured HspR was renatured, the protein gained optimal activity only if one of these GroEL class chaperones was present along with DnaK. The renaturation process was found to be dependent on ATP hydrolysis. The DnaK-dependent DNA-binding activity of HspR could also be stimulated by DnaJ, but GrpE, which is known to release DnaK-bound substrates, was found to be inhibitory. The results of this study suggest that protein folding plays a substantial role in the activation of HspR following heat shock and that DnaK may be involved in two ways – first, as a chaperone acting in concert with GroEL and/or DnaJ and second, as a co-repressor bound to HspR.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/012294-0
2008-02-01
2020-10-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/2/484.html?itemId=/content/journal/micro/10.1099/mic.0.2007/012294-0&mimeType=html&fmt=ahah

References

  1. Babst M., Hennecke H., Fischer H. M.. 1996; Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum . Mol Microbiol19:827–839
    [Google Scholar]
  2. Bahl H., Muller H., Behrens S., Joseph H., Narberhaus F.. 1995; Expression of heat shock genes in Clostridium acetobutylicum . FEMS Microbiol Rev17:341–348
    [Google Scholar]
  3. Basu A., Chawla-Sarkar M., Chakrabarti S., Das Gupta S. K.. 2002; Origin binding activity of the mycobacterial plasmid pAL5000 replication protein RepB is stimulated through interactions with host factors and coupled expression of repA . J Bacteriol184:2204–2214
    [Google Scholar]
  4. Brehmer D., Gassler C., Rist W., Mayer M. P., Bukau B.. 2004; Influence of GrpE on DnaK–substrate interactions. J Biol Chem279:27957–27964
    [Google Scholar]
  5. Bucca G., Brassington A. M., Schonfeld H. J., Smith C. P.. 2000; The HspR regulon of Streptomyces coelicolor : a role for the DnaK chaperone as a transcriptional co-repressor. Mol Microbiol38:1093–1103
    [Google Scholar]
  6. Bucca G., Brassington A. M., Hotchkiss G., Mersinias V., Smith C. P.. 2003; Negative feedback regulation of dnaK , clpB and lon expression by the DnaK chaperone machine in Streptomyces coelicolor , identified by transcriptome and in vivo DnaK-depletion analysis. Mol Microbiol50:153–166
    [Google Scholar]
  7. Bukau B.. 1993; Regulation of the Escherichia coli heat-shock response. Mol Microbiol9:671–680
    [Google Scholar]
  8. Georgopoulos C., Liberek K., Zylicz M., Ang D.. 1994; Properties of the heat shock proteins of Escherichia coli and the autoregulation of the heat-shock response. In The Biology of Heat Shock Proteins and Molecular Chaperones pp209–249 Edited by Morimoto A. T. R. I., Georgopoulos C. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  9. Goyal K., Qamra R., Mande S. C.. 2006; Multiple gene duplication and rapid evolution in the groEL gene: functional implications. J Mol Evol63:781–787
    [Google Scholar]
  10. Grandvalet C., de Crecy-Lagard V., Mazodier P.. 1999; The ClpB ATPase of Streptomyces albus G belongs to the HspR heat shock regulon. Mol Microbiol31:521–532
    [Google Scholar]
  11. Liberek K., Wall D., Georgopoulos C.. 1995; The DnaJ chaperone catalytically activates the DnaK chaperone to preferentially bind the sigma 32 heat shock transcriptional regulator. Proc Natl Acad Sci U S A92:6224–6228
    [Google Scholar]
  12. Lindquist S., Craig E. A.. 1988; The heat-shock proteins. Annu Rev Genet22:631–677
    [Google Scholar]
  13. Mayhew M., da Silva A. C., Martin J., Erdjument-Bromage H., Tempst P., Hartl F. U.. 1996; Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature379:420–426
    [Google Scholar]
  14. Qamra R., Srinivas V., Mande S. C.. 2004; Mycobacterium tuberculosis GroEL homologues unusually exist as lower oligomers and retain the ability to suppress aggregation of substrate proteins. J Mol Biol342:605–617
    [Google Scholar]
  15. Raina S., Missiakas D., Georgopoulos C.. 1995; The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli . EMBO J14:1043–1055
    [Google Scholar]
  16. Rouviere P. E., De Las Penas A., Mecsas J., Lu C. Z., Rudd K. E., Gross C. A.. 1995; rpoE , the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli . EMBO J14:1032–1042
    [Google Scholar]
  17. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  18. Schulz A., Schumann W.. 1996; hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol178:1088–1093
    [Google Scholar]
  19. Segal G., Ron E. Z.. 1996; Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat. J Bacteriol178:3634–3640
    [Google Scholar]
  20. Stewart G. R., Snewin V. A., Walzl G., Hussell T., Tormay P., O'Gaora P., Goyal M., Betts J., Brown I. N., Young D. B.. 2001; Overexpression of heat-shock proteins reduces survival of Mycobacterium tuberculosis in the chronic phase of infection. Nat Med7:732–737
    [Google Scholar]
  21. Stewart G. R., Wernisch L., Stabler R., Mangan J. A., Hinds J., Laing K. G., Young D. B., Butcher P. D.. 2002; Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology148:3129–3138
    [Google Scholar]
  22. Stewart G. R., Robertson B. D., Young D. B.. 2003; Tuberculosis: a problem with persistence. Nat Rev Microbiol1:97–105
    [Google Scholar]
  23. Stewart G. R., Newton S. M., Wilkinson K. A., Humphreys I. R., Murphy H. N., Robertson B. D., Wilkinson R. J., Young D. B.. 2005; The stress-responsive chaperone alpha-crystallin 2 is required for pathogenesis of Mycobacterium tuberculosis . Mol Microbiol55:1127–1137
    [Google Scholar]
  24. Wilkinson K. A., Stewart G. R., Newton S. M., Vordermeier H. M., Wain J. R., Murphy H. N., Horner K., Young D. B., Wilkinson R. J.. 2005; Infection biology of a novel alpha-crystallin of Mycobacterium tuberculosis : Acr2. J Immunol174:4237–4243
    [Google Scholar]
  25. Yura T., Nagai H., Mori H.. 1993; Regulation of the heat-shock response in bacteria. Annu Rev Microbiol47:321–350
    [Google Scholar]
  26. Zuber U., Schumann W.. 1994; CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis . J Bacteriol176:1359–1363
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/012294-0
Loading
/content/journal/micro/10.1099/mic.0.2007/012294-0
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