1887

Microbiology Society logo

Volume 146, Issue 4

Cellular lipid composition influences stress activation of the yeast general stress response element (STRE)

This paper is dedicated to my parents Sandhya and Samir.

Free

Abstract

The heat inducibility of the yeast heat-shock response (HSR) pathway has been shown to be critically dependent on the level of unsaturated fatty acids present in the cell. Here the inducibility by heat or salt of the independently regulated general stress response (GSR) pathway is shown to be affected in the same way. An increase in the percentage of unsaturated fatty acids in heat- or salt-acclimated cells correlated with a decrease in the induction of a general stress-response-promoter-element (STRE)-driven reporter gene by either stress. Despite inducing reporter gene expression, sorbic acid treatment did not confer salt cross-tolerance on the cells. This failure correlated with a failure to increase the percentage of unsaturated fatty acids in the cells, suggesting that GSR pathway induction, in the absence of lipid changes, is insufficient for the induction of cross-tolerance. Cells grown with fatty acid supplements under anaerobic conditions provided further evidence for a potential role for lipids in the acquisition of stress resistance. These cells contained different fatty acid profiles depending on the fatty acid supplement supplied, exhibited differential sensitivity to both heat and salt stress, but had not undergone STRE induction. These results suggest that heat- and salt-stress induction of the GSR are sensitive to the level of unsaturated fatty acids present in the cell and that stress cross-tolerance may be a lipid-mediated phenomenon. Given that an increased level of unsaturated fatty acids also down-regulates heat induction of the HSR pathway, these observations lead to the provocative hypothesis that lipid modifications, rather than HSR or GSR pathway induction, are a major contributor to the induced heat and salt tolerance of yeast cells.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): general stress response , GSR, general stress response , HSE, heat-shock element , HSR, heat-shock response , HSTF, heat-shock transcription factor , lipids , STRE , STRE, general stress response promoter element and yeast
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-4-877
2000-04-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/4/1460877a.html?itemId=/content/journal/micro/10.1099/00221287-146-4-877&mimeType=html&fmt=ahah

References

  1. Carratu L., Franceschelli S., Pardini C. L., Kobayashi G. S., Horvath I., Vigh L., Maresca B. 1996; Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93:3870–3875 [CrossRef]
     [Google Scholar]
  2. Chatterjee M. T., Khalawan S. A., Curran B. P. G. 1997; Alterations in cellular lipids may be responsible for the transient nature of the yeast heat shock response. Microbiology 143:3063–3068 [CrossRef]
     [Google Scholar]
  3. Coote P. J., Jones M. V., Seymour I. J., Rowe D. L., Ferdinando D. P., McArthur A. J., Cole M. B. 1994; Activity of plasma membrane H+-ATPase is a key physiological determinant of thermotolerance in Saccharomyces cerevisiae. Microbiology 140:1881–1890 [CrossRef]
     [Google Scholar]
  4. Curran B. P. G., Khalawan S. A. 1994; Alcohols lower the threshold temperature for the maximal activation of a heat shock expression vector in the yeast Saccharomyces cerevisiae. Microbiology 140:2225–2228 [CrossRef]
     [Google Scholar]
  5. Horvath I., Glatz A., Varvasovszki V.8 other authors 1998; Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a ‘fluidity gene’. Proc Natl Acad Sci USA 95:3513–3518 [CrossRef]
     [Google Scholar]
  6. Hossack J. A., Rose A. H. 1976; Fragility of plasma membranes in Saccharomyces cerevisiae enriched with different sterols. J Bacteriol 127:67–75
     [Google Scholar]
  7. Inoue K., Matsuzaki H., Matsumoto K., Shibuya I. 1997; Unbalanced membrane phospholipid compositions affect transcriptional expression of certain regulatory genes in Escherichia coli. J Bacteriol 179:2872–2878
     [Google Scholar]
  8. Kamada Y., Jung U. S., Piotrowski J., Levin D. E. 1995; The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9:1559–1571 [CrossRef]
     [Google Scholar]
  9. Kobayashi N., McEntee K. 1990; Evidence for a heat shock transcription factor-independent mechanism for heat shock induction of transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 87:6550–6554 [CrossRef]
     [Google Scholar]
  10. Kobayashi N., McEntee K. 1993; Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13:248–256
     [Google Scholar]
  11. Lindquist S. 1986; The heat shock response. Annu Rev Biochem 55:1151–1191 [CrossRef]
     [Google Scholar]
  12. Mager W. H., De Kruijff A. J. J. 1995; Stress-induced transcriptional activation. Microbiol Rev 59:506–531
     [Google Scholar]
  13. Marchler G., Schüller C., Adam G., Ruis H. 1993; A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12:1997–2003
     [Google Scholar]
  14. Martinez-Pastor M. T., Marchler G., Schüller C., Marchler-Bauer A., Ruis H., Estruch F. 1996; The Saccharomyces cerevisiae zinc finger proteins Msn2p & Msn4p are required for transcriptional induction through the stress-response element (STRE). EMBO J 15:2227–2235
     [Google Scholar]
  15. Panaretou B., Piper P. W. 1990; Plasma-membrane ATPase action affects several stress tolerances of Saccharomyces cerevisiae and Schizosaccharomyces pombe as well as the extent and duration of the heat shock response. J Gen Microbiol 136:1763–1770 [CrossRef]
     [Google Scholar]
  16. Parsell D. A., Lindquist S. 1993; The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496 [CrossRef]
     [Google Scholar]
  17. Pelham H. R. B., Bienz M. 1982; A synthetic heat shock promoter element confers heat-inducibility on the herpes-simplex virus thymidine kinase gene. EMBO J 1:1473–1477
     [Google Scholar]
  18. Piper P. W. 1993; Molecular events associated with the acquisition of heat tolerance in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 11:1–11 [CrossRef]
     [Google Scholar]
  19. Ruis H., Schüller C. 1995; Stress signalling in yeast. Bioessays 17:959–965 [CrossRef]
     [Google Scholar]
  20. Schüller C., Brewster J. L., Alexander M. R., Gustin M. C., Ruis H. 1994; The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J 13:4382–4389
     [Google Scholar]
  21. Sorger P. K., Pelham H. R. B. 1988; Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864 [CrossRef]
     [Google Scholar]
  22. Thomas S., Hossack J. A., Rose A. H. 1978; Plasma-membrane lipid composition and ethanol tolerance in Saccharomyces cerevisiae. Arch Microbiol 117:239–245 [CrossRef]
     [Google Scholar]
  23. Varela J. C. S., Praekelt U. M., Meacock P. A., Planta R. J., Mager W. H. 1995; The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol 15:6232–6245
     [Google Scholar]
  24. Vigh L., Maresca B., Harwood J. L. 1998; Does the membrane’s physical state control the expression of heat shock and other genes?. Trends Biochem Sci 10:369–374
     [Google Scholar]
  25. Wiederrecht G., Seto D., Parker C. S. 1988; Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54:841–853 [CrossRef]
     [Google Scholar]
  26. Wieser R., Adam G., Wagner A., Schüller C., Marchler G., Ruis H., Krawiec Z., Bilinski T. 1991; Heat shock factor-independent heat control of transcription of the CTT1 gene encoding the cytosolic catalase T of Saccharomyces cerevisiae. J Biol Chem 266:12406–12411
     [Google Scholar]
  27. Winderickx J., De Winde J. H., Crauwels M., Hino A., Hohmann S., Van Dijck P., Thevelein J. M. 1996; Regulation of genes encoding sub-units of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control?. Mol Gen Genet 252:470–482
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-4-877
Loading
Cellular lipid composition influences stress activation of the yeast general stress response element (STRE)This paper is dedicated to my parents Sandhya and Samir.
Microbiology 146, 877 (2000); https://doi.org/10.1099/00221287-146-4-877
/content/journal/micro/10.1099/00221287-146-4-877
/content/journal/micro/10.1099/00221287-146-4-877
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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