Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli

Molecular Microbiology

Volumn 30, Issue 3, 1998, Pages 567-581

  Tomoyasu, Toshifumi ^a   Ogura, Teru ^b   Tatsuta, Takashi ^b   Bukau, Bernd ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; BACTERIAL PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN; LUCIFERASE; PROTEINASE; RNA POLYMERASE; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME STABILITY; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HEAT SHOCK; HOMEOSTASIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DENATURATION; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

ATP-DEPENDENT PROTEASES; BACTERIAL PROTEINS; CELL SURVIVAL; DNA-DIRECTED RNA POLYMERASES; ENZYME INDUCTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GROEL PROTEIN; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; LUCIFERASES; MEMBRANE PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN FOLDING; SIGMA FACTOR;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0031793242     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.01090.x     Document Type: Article

References (55)

1. Abravaya, K., Myers, M.P., Murphy, S.P., and Morimoto, R.I. (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6: 1153-1164.
2. Ananthan, J., Goldberg, A.L., and Voellmy, R. (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232: 522-524.
3. Berlyn, M.K.B., Low, K.B., Rudd, K.E., and Singer, M. (1996) Linkage map of Escherichia coli K-12. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1715-1902.
4. Bukau, B. (1993) Regulation of the E. coli heat shock response. Mol Microbiol 9: 671-680.
5. Bukau, B., and Walker, G. (1990) Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J 9: 4027-4036.
6. Chaudhury, A.M., and Smith, G.R. (1984) A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination. Proc Natl Acad Sci USA 81: 7850-7854.
7. Craig, E.A., and Gross, C.A. (1991) Is hsp70 the cellular thermometer? Trends Biochem Sci 16: 135-140.
8. 32. Cell 69: 833-842.
9. 32. EMBO J 15: 607-617.
10. Georgopoulos, C., Liberek, K., Zylicz, M., and Ang, D. (1994) Properties of the heat shock proteins of Escherichia coli and the autoregulation of the heat shock response. In Properties of the Heat Shock Proteins of Escherichia coli and the Autoregulation of the Heat Shock Response. Morimoto, R.I., Tissières, A., and Georgopoulos, C. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 209-250.
11. Gething, M.-J.H., and Sambrook, J.F. (1992) Protein folding in the cell. Nature 355: 33-45.
12. Goff, S.A., and Goldberg, A.L. (1985). Production of abnormal proteins in E. coli stimulates transcription of Ion and other heat shock genes. Cell 4: 587-595.
13. Gottesman, S., Maurizi, M.R., and Wickner, S. (1997a) Regulatory subunits of energy-dependent proteases. Cell 91: 435-438.
14. Gottesman, S., Wickner, S., and Maurizi, M.R. (1997b) Protein quality control: triage by chaperones and proteases. Genes Dev 11: 815-823.
15. Gross, C.A. (1996) Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1382-1399.
16. BAD promoter. J Bacteriol 177: 4121-4130.
17. Halladay, J.T., and Craig, E.A. (1995) A heat shock transcription factor with reduced activity suppresses a yeast HSP70 mutant. Mol Cell Biol 15: 4890-4897.
18. Hartl, F.U. (1996). Molecular chaperones in cellular protein folding. Nature 381: 571-580.
19. Herbst, R., Schafer, U., and Seckler, R. (1997). Equilibrium intermediates in the reversible unfolding of firefly (Photinus pyralis) luciferase. J Biol Chem 272: 7099-7105.
20. 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc Natl Acad Sci USA 92: 3516-3520.
21. Hesterkamp, T., and Bukau, B. (1998) Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E. coli. EMBO J 17: 4818-4828.
22. 32 in Escherichia coli. J Bacteriol 176: 5648-5653.
23. 32 and abnormal proteins in Escherichia coli. J Bacteriol 179: 7219-7225.
24. Kim, D., Ouyang, H., and Li, G.C. (1995) Heat shock protein hsp70 accelerates the recovery of heat-shocked mammalian cells through its modulation of heat shock transcription factor HSF1. Proc Natl Acad Sci USA 92: 2126-2130.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
26. Lanzer, M. (1988) Untersuchungen zur Kompetition zwischen Repressor und RNA - Polymerase um DNA - Bindungsorte. University of Heidelberg, Heidelberg, Germany.
27. Liberek, K., and Georgopoulos, C. (1993) Autoregulation of the Escherichia coli heat shock response by the DnaK and DnaJ heat shock proteins. Proc Natl Acad Sci USA 90: 11019-11023.
28. 32 transcription factor. Proc Natl Acad Sci USA 89: 3516-3520.
29. Lowe, P.A., Hager, D.A., and Burgess, R.R. (1978). Purification and properties of the σ subunit of Escherichia coli DNA-dependent RNA polymerase. Biochemistry 18: 1344-1352.
30. 2 regulatory elements. Nucleic Acids Res 25: 1203-1210.
31. 32, constitutes a DnaK binding site and is conserved among eubacteria. J Mol Biol 256: 829-837.
32. Mifflin, L.C., and Cohen, R.E. (1994) Characterization of denatured protein inducers of the heat shock (stress) response in Xenopus laevis oocytes. J Biol Chem 269: 15710-15717.
33. Morimoto, R.I. (1993). Cell in stress: transcriptional activation of heat shock genes. Science 269: 1409-1410.
34. Morimoto, R.I., Kroeger, P.E., and Cotto, J.J. (1996) The transcriptional regulation of heat shock genes: a plethora of heat shock factors and regulatory conditions. In The Transcriptional Regulation of Heat Shock Genes: A Plethora of Heat Shock Factors and Regulatory Conditions. Feige, U., Morimoto, R.I., Yahara, I., and Polla, B.S. (eds). Basle: Birkhäuser-Verlag, pp. 139-163.
35. Mosser, D.D., Duchaine, J., and Massie, B. (1993) The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol 13: 5427-5438.
36. Neidhardt, F.C. (1987). Chemical composition of Escherichia coli. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular biology. Neidhardt, F.C., Ingraham, J.L., Low, K.B., Magasanik, B., Schaechter, M., and Umbarger, H.E. (eds). Washington, DC: American Society for Microbiology Press, pp. 3-6.
37. Nover, L. (1991) Inducers of HSP synthesis: heat shock and chemical sensors. In Inducers of HSP Synthesis: Heat Shock and Chemical Sensors. Nover, L. (ed.). Boca Raton, FL: CRC Press, pp. 5-41.
38. Packschies, L., Theyssen, H., Buchberger, A., Bukau, B., Goody, R.S., and Reinstein, J. (1997) GrpE accelerates nucleotide exchange of the molecular chaperone DnaK with an associative displacement mechanism. Biochemistry 36: 3417-3422.
39. Parsell, D., and Sauer, R.T. (1989) Induction of a heat shock-like response by unfolded protein in Escherichia coli: dependence on protein level not protein degradation. Genes Dev 3: 1226-1232.
40. Qu, J.-N., Makino, S.-I., Adachi, H., Koyama, Y., Akiyama, Y., Ito, K., Tomoyasu, T., et al. (1996) The tolZ Gene of Escherichia coli is identified as the ftsH gene. J Bacteriol 178: 3457-3461.
41. Rüdiger, S., Buchberger, A., and Bukau, B. (1997a) Interaction of Hsp70 chaperones with substrates. Nature Struct Biol 4: 342-349.
42. Rüdiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997b) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16: 1501-1507.
43. Schröder, H., Langer, T., Hartl, F.-U., and Bukau, B. (1993) DnaK, DnaJ, GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J 12: 4137-4144.
44. Shi, Y., Mosser, D.D., and Morimoto, R.I. (1998) Molecular chaperones as HSF-specific transcriptional repressors. Genes Dev 12: 654-666.
45. 32. Nature 329: 348-350.
46. 32 is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes Dev 3: 2003-2010.
47. 32. Genes Dev 4: 2202-2209.
48. Szabo, A., Korzun, R., Hartl, F.U., and Flanagan, J. (1996) A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J 15: 408-417.
49. Takeshita, S., Sato, M., Toba, M., Masahashi, W., and Hashimoto-Gotoh, T. (1987) High- copy-number and low-copy-number plasmid vectors for lacZ α-complementation and chloramphenicol- or kanamycin-resistance selection. Gene 61: 63-74.
50. Tilly, K., McKittrick, N., Zylicz, M., and Georgopoulos, C. (1983) The DnaK protein modulates the heat-shock response of Escherichia coli. Cell 34: 641-646.
51. 32. J Bacteriol 171: 1585-1589.
52. 32. EMBO J 14: 2551-2560.
53. Voellmy, R. (1996) Sensing stress and responding to genes. In Sensing Stress and Responding to Genes. Feige, U., Morimoto, R.I., Yahara, I., and Polla, B.S. (eds). Basle: Birkhäuser-Verlag, pp. 121-137.
54. Wild, J., Walter, W.A., Gross, C.A., and Altman, E. (1993) Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J Bacteriol 175: 3992-3997.
55. Yura, T., Nagai, H., and Mori, H. (1993) Regulation of the heat-shock response in bacteria. Annu Rev Microbiol 47: 321-350.