Advertisement

The role of heat-shock proteins in thermotolerance

Chapter

Summary

The role of heat-shock proteins (hsps) in thermotolerance was examined in the budding yeast Saccharomyces cerevisiae and in the fruit fly Drosophila melanogaster. In yeast cells, the major protein responsible for thermotolerance is hsp 100. In cells carrying mutations in the hsp 100 gene, HSP 104, growth is normal at both high and low temperatures, but the ability of cells to survive extreme temperatures is severely impaired. The loss of thermotolerance is apparently due to the absence of the hsp 104 protein itself because, with the exception of the hsp 104 protein, no differences in protein profiles were observed between mutant and wild-type cells. Aggregates found in mutant cells at high temperatures suggest that the cause of death may be the accumulation of denatured proteins. No differences in the rates of protein degradation were observed between mutant and wild-type cells. This, and genetic analysis of cells carrying multiple hsp 70 and hsp 104 mutations, suggests that the primary function of hsp 104 is to rescue proteins from denaturation rather than to degrade them once they have been denatured. Drosophila cells do not produce a protein in the hsp 100 class in response to high temperatures. In this organism, hsp 70 appears to be the primary protein involved in thermotolerance. Thus, the relative importance of different hsps in thermotolerance changes from organism to organism.

Keywords

Yeast Cell Mutant Cell Nurse Cell Yeast Protein Sodium Arsenite 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Carper, S.W., Duffy, J.J. & Gerner, E.W. 1987 Heat shock proteins in thermotolerance and other cellular processes. Cancer Res. 47, 5249–5255.PubMedGoogle Scholar
  2. Craig, E.A. & Jacobsen, K. 1984 Mutations of the heat inducible 70 kilodalton genes of yeast confer temperature sensitive growth. Cell 38, 841–849.PubMedCrossRefGoogle Scholar
  3. Craig, E.A. & McCarthy, B.J. 1980 Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucl. Acids Res. 8, 4441–4457.PubMedCrossRefGoogle Scholar
  4. Daufeldt, J.A. & Harrison, H.H. 1984 Quality control and technical outcome of two-dimensional electrophoresis in a clinical laboratory setting. Clin. Chem. 30, 1972–1980.PubMedGoogle Scholar
  5. Etyan, E., Ganoth, D., Armon, T. & Hershko, A. 1989 ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. Proc. natn. Acad. Sci. U.S.A. 86, 7751–7755.CrossRefGoogle Scholar
  6. Feder, J.H., Rossi, J.M., Solomon, J., Solomon, N. & Lindquist, S. 1992 The consequences of expressing hsp 70 in Drosophila cells at normal temperatures. Genes Dev. 6, 1402–1413.PubMedCrossRefGoogle Scholar
  7. Finley, D., Ozkaynak, E. & Varshavsky, A. 1987 The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48, 1035–1046.PubMedCrossRefGoogle Scholar
  8. Georgopoulos, C. 1992 The emergence of the chaperone machines. Trends Biochem. Sci. 17, 295–299.PubMedCrossRefGoogle Scholar
  9. Gething, M.-J. & Sambrook, J. 1992 Protein folding in the cell. Nature, Lond. 355, 33–45.CrossRefGoogle Scholar
  10. Golic, K.G. & Lindquist, S. 1989 The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509.PubMedCrossRefGoogle Scholar
  11. Gottesman, S., Squires, C, Pichersky, E., Carrington, M., Hobbs, M., Mattick, J.S., Dalrymple, B., Kuramitsu, H., Shiroza, T. & Foster, T. 1990 Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc. natn. Acad. Sci. U.S.A. 87, 3513–3517.CrossRefGoogle Scholar
  12. Katayama, Y., Gottesman, S., Pumphery, J., Rudikoff, S., Clarkand, W.P. & Maurizi, M.R. 1988 The two-component, ATP-dependent Cip protease of Escherichia coli. J. biol. Chem. 263, 15226–15236.PubMedGoogle Scholar
  13. Kitagawa, M., Wada, C, Yoshioka, S. & Yura, T. 1991 Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock σ factor (σ32). J. Bacteriol. 173, 4247–4253.PubMedGoogle Scholar
  14. Lindquist, S. 1980 Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev. Biol. 77, 463–479.PubMedCrossRefGoogle Scholar
  15. Lindquist, S. 1986 The heat-shock response. A. Rev. Biochem. 55, 1151–1191.CrossRefGoogle Scholar
  16. Lindquist, S. & Craig, E.A. 1986 The heat-shock proteins. A. Rev. Genet. 22, 631–677.CrossRefGoogle Scholar
  17. Nover, L. 1991 Heat shock response, 1st edn. Boca Raton, Florida: CRC Press.Google Scholar
  18. Parsell, D.A., Sanchez, Y., Stitzel, J.D. & Lindquist, S. 1991 Hsp 104 is a highly conserved protein with two essential nucleotide-binding sites. Nature, Lond. 353, 270–273.CrossRefGoogle Scholar
  19. Pelham, H.R. 1986 Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46, 959–961.PubMedCrossRefGoogle Scholar
  20. Sanchez, Y. & Lindquist, S.L. 1990 HSP 104 required for induced thermotolerance. Science, Wash. 248, 1112–1115.CrossRefGoogle Scholar
  21. Sanchez, Y., Taulien, J., Borkovich, K. & Lindquist, S.L. 1990 Hsp 104 is required for tolerance to many forms of stress. Science, Wash. 248, 1112–1115.CrossRefGoogle Scholar
  22. Sanchez, Y., Parsell, D.A., Taulien, J., Vogel, Craig, E.A. & Lindquist, S.L. 1993 Genetic evidence for a functional relationship between hsp 104 and hsp 70. (In preparation.)Google Scholar
  23. Seufert, W. & Jentsch, S. 1990 Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 9, 543–550.PubMedGoogle Scholar
  24. Solomon, J.M., Rossi, J.M., Golic, K., McGarry, T. & Lindquist, S. 1991 Changes in Hsp 70 Alter Thermotolerance and Heat-Shock Regulation in Drosophila. New Biol. 3, 1106–1120.PubMedGoogle Scholar
  25. Squires, C.L., Pedersen, S., Ross, B.M. & Squires, C. 1991 ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 173, 4254–4262.PubMedGoogle Scholar
  26. Welte, M.A., Tetrault, J. & Lindquist, S. 1993 A new method for manipulating transgenes: improving thermotolerance in Drosophila embryos. (In preparation.)Google Scholar
  27. Werner, W.M., Stone, D.E. & Craig, E.A. 1987 Complex interactions among members of an essential subfamily of hsp 70 genes in Saccharomyces cerevisiae. Molec. Cell Biol. 7, 2568–2577.Google Scholar
  28. Zimmerman, J.L. & Cohill, P.R. 1991 Heat shock and thermotolerance in plant and animal embryogenesis. New Biol 3, 641–650.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1993

Authors and Affiliations

There are no affiliations available

Personalised recommendations