1887

Microbiology Society logo

Volume 137, Issue 7

Induction of increased thermotolerance in may be triggered by a mechanism involving intracellular pH Free

Abstract

Summary: Incubation of at sub-lethal temperatures results in an increase in thermotolerance. This process is dependent not only on the sub-lethal temperature but also on the duration of sub-lethal heating. This indicates that the mechanism inducing thermotolerance is a time/temperature dose response. Other factors that induce thermotolerance include exposure to ethanol, sorbic acid and low external pH values. These factors induce thermotolerance after incubation in the presence of protein synthesis inhibitors, and they are all known to affect the intracellular pH (pH). The acquisition of increased thermotolerance is minimal with sub-lethal heating under neutral external pH conditions. However, when the external pH is reduced to 4·0 the level of induced thermotolerance increases to a maximum value. Using a specific ATPase inhibitor, diethylstilboestrol (DES), ATPase activity was shown to be essential for the cell to survive heat stress. In addition, measurement of acid efflux, or ATPase activity, revealed that proton pumping from the cell increased by approximately 50% at sublethal temperatures that induce thermotolerance. This work has clearly implicated pH perturbation as the triggering mechanism conferring thermotolerance on .

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-137-7-1701
1991-07-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/137/7/mic-137-7-1701.html?itemId=/content/journal/micro/10.1099/00221287-137-7-1701&mimeType=html&fmt=ahah

References

  1. Ashburner M., Bonner J. J. 1979; The induction of gene activity in Drosophila by heat shock.. Cell 17:241–254
     [Google Scholar]
  2. Barnes C. A., Johnston G. C., Singer R. A. 1990; Thermotolerance is independent of induction of the full spectrum of heat shock proteins and of cell cycle blockage in the yeast Saccharomyces cerevisiae . Journal of Bacteriology 172:4352–4358
     [Google Scholar]
  3. Borkovich K. A., Farrelly F. W., Finkelstein D. B., Tanlien J., Lindquist S. 1989; Hsp 82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures.. Molecular and Cellular Biology 9:3919–3930
     [Google Scholar]
  4. Busa W. B., Nuccitelli R. 1984; Metabolic regulation via intracellular pH.. American Journal of Physiology 246:409–438
     [Google Scholar]
  5. Cole M. B., Keenan M. H. J. 1987; Effects of weak acids and external pH on the intracellular pH of Zygosaccharomyces bailii, and its implications in weak-acid resistance.. Yeast 3:23–32
     [Google Scholar]
  6. Conway E. J., Downey M. 1950; pH values of the yeast cell.. Biochemical Journal 47:355–360
     [Google Scholar]
  7. Coote P. J., Cole M. B., Holyoak C. 1991; Thermal inactivation of Listeria monocytogenes during a process simulating temperatures achieved during microwave heating.. Journal of Applied Bacteriology (in the Press) 70:
     [Google Scholar]
  8. Eilam Y., Lavi H., Grossowicz N. 1984; Effects of inhibitors of plasma membrane ATPase on potassium and calcium fluxes, membrane potential and protonmotive force in the yeast Saccharomyces cerevisiae . Microbios 41:177–189
     [Google Scholar]
  9. Eraso P., Gancedo C. 1987; Activation of yeast plasma membrane ATPase by acid pH during growth.. FEBS Letters 224:187–192
     [Google Scholar]
  10. Farber J. M., Brown B. E. 1990; Effect of prior heat shock on heat resistance of Listeria monocytogenes in meat.. Applied and Environmental Microbiology 56:1584–1587
     [Google Scholar]
  11. Finkelstein D. B., Strausberg S. 1983; Identification and expression of a cloned yeast heat shock gene.. Journal of Biological Chemistry 258:1908–1913
     [Google Scholar]
  12. Finley D., Ozkaynak E., Vashavsky A. 1987; The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation and other stresses.. Cell 48:1035–1046
     [Google Scholar]
  13. Gillies R. J., Ugurbil K., den Hollander J. A., Shulman R. G. 1981; 33P NMR studies of intracellular pH and phosphate metabolism during the cell division cycle of Saccharomyces cerevisiae . Proceedings of the National Academy of Sciences of the United States of America 78:2125–2129
     [Google Scholar]
  14. Goffeau A., Slayman C. W. 1981; The proton-translocating ATPase of the fungal plasma membrane.. Biochimica et Biophysica Acta 639:197–223
     [Google Scholar]
  15. Hall B. G. 1983; Yeast thermotolerance does not require protein synthesis.. Journal of Bacteriology 156:1363–1365
     [Google Scholar]
  16. Krebs H. A., Wiggins D., Stubbs M., Sols A., Bedoya F. 1983; Studies on the mechanism of the antifungal action of benzoate.. Biochemical Journal 214:657–663
     [Google Scholar]
  17. Iida H. 1988; Multistress resistance of Saccharomyces cerevisiae is generated by insertion of retrotransposon Ty into the 5' coding region of the adenylate cyclase gene.. Molecular and Cellular Biology 8:5555–5560
     [Google Scholar]
  18. Leao C., van Uden N. 1984; Effects of ethanol and other alkanols on passive proton influx in the yeast Saccharomyces cerevisiae . Biochimica et Biophysica Acta 774:43–48
     [Google Scholar]
  19. Levinson W., Opperman H., Jackson J. 1980; Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells.. Biochimica et Biophysica Acta 606:170–180
     [Google Scholar]
  20. Li G. C, Shiu E. C., Hahn G. M. 1980; Similarities in cellular inactivation by hyperthermia or by ethanol.. Radiation Research 82:257–268
     [Google Scholar]
  21. Lindquist S. 1986; The heat shock response.. Annual Review of Biochemistry 55:1151–1191
     [Google Scholar]
  22. Lindquist S., Craig E. A. 1988; The heat shock proteins.. Annual Review of Genetics 22:631–677
     [Google Scholar]
  23. Mackey B. M., Derrick C. M. 1986; Elevation of the heat resistance of Salmonella typhimurium by sublethal heat shock.. Journal of Applied Bacteriology 61:389–393
     [Google Scholar]
  24. Mackey B. M., Derrick C. M. 1987; The effect of prior heat shock on the thermoresistance of Salmonella thompson in foods.. Letters in Applied Microbiology 5:115–118
     [Google Scholar]
  25. Macris B. J. 1975; Mechanism of benzoic acid uptake by Saccharomyces cerevisiae . Applied Microbiology 30:503–506
     [Google Scholar]
  26. Malpartida F., Serrano R. 1981; Proton translocation catalyzed by the purified yeast plasma membrane ATPase reconstituted in liposomes.. FEBS Letters 131:351–354
     [Google Scholar]
  27. McAlister L., Finkelstein D. B. 1980; Heat shock proteins and thermal resistance in yeast.. Biochemical and Biophysical Research Communications 93:819–824
     [Google Scholar]
  28. 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.. Journal of General Microbiology 136:1763–1770
     [Google Scholar]
  29. Petko L., Lindquist S. 1986; Hsp 26 is not required for growth at high temperatures; nor for thermotolerance, spore development, or germination.. Cell 45:885–894
     [Google Scholar]
  30. Piper P. W. 1990; Interdépendance of several heat shock gene activations, cyclic AMP decline and changes at the plasma membrane of Saccharomyces cerevisiae . Antonie van Leeuwenhoek 58:195–201
     [Google Scholar]
  31. Piper P. W., Curran B., Davies M. W., Lockheart A., Reid G. 1986; Transcription of the phosphoglycerate kinase gene of Saccharomyces cerevisiae increases when fermentative cultures are stressed by heat shock.. European Journal of Biochemistry 161:525–531
     [Google Scholar]
  32. Plesofsky-Vig N., Brambl R. 1985; Heat shock response of Neurospora crassa : protein synthesis and induced thermotolerance.. Journal of Bacteriology 162:1083–1091
     [Google Scholar]
  33. Plesset J., Palm C., McLaughlin C. S. 1982; Induction of heat shock proteins and thermotolerance by ethanol in Saccharomyces cerevisiae . Biochemical and Biophysical Research Communications 108:1340–1345
     [Google Scholar]
  34. Riemersma J. C., Alsbach E. J. J. 1974; Proton translocation during anaerobic energy production in Saccharomyces cerevisiae . Biochimica et Biophysica Acta 339:274–284
     [Google Scholar]
  35. Ryan J. P., Ryan H. 1972; The role of intracellular pH in the regulation of cation exchange in yeast.. Biochemical Journal 128:139–146
     [Google Scholar]
  36. Sanchez Y., Lindquist S. L. 1990; HSP104 required for induced thermotolerance.. Science 248:1112–1115
     [Google Scholar]
  37. Serrano R. 1980; Effect of ATPase inhibitors on the proton pump of respiratory deficient yeast.. European Journal of Biochemistry 105:419–424
     [Google Scholar]
  38. Sigler K., Kotyk A., Knotkova A., Opekarova M. 1981; Processes involved in the creation of buffering capacity and in substrate-induced proton extrusion in the yeast Saccharomyces cerevisiae . Biochimica et Biophysica Acta 643:583–592
     [Google Scholar]
  39. Suomalainen H., Oura E. 1955; Buffer effect in fermentation solutions.. Experimental Cell Research 9:355–359
     [Google Scholar]
  40. Watson K., Dunlop G., Cavicchioli R. 1984; Mitochondrial and cytoplasmic protein synthesis are not required for heat shock acquisition of ethanol and thermotolerance in yeast.. FEBS Letters 172:299–302
     [Google Scholar]
  41. Weitzel G., Pilatus U., Rensing L. 1987; The cytoplasmic pH, ATP content and total protein synthesis rate during heat-shock protein inducing treatments in yeast.. Experimental Cell Research 170:64–79
     [Google Scholar]
  42. White F. P., Currie R. W. 1982; A mammalian response to trauma: the synthesis of a 71-kD protein.. Heat Shock: From Bacteria to Man379–386 Schlesinger M. J., Ashburner A., Tissieres A. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  43. Willsky G. R. 1979; Characterisation of the plasma membrane Mg2+-ATPase from the yeast Saccharomyces cerevisiae . Journal of Biological Chemistry 254:3326–3332
     [Google Scholar]
  44. Yamamori T., Yura T. 1982; Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K.12. Proceedings of the National Academy of Sciences of the United States of America 79:860–864
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-137-7-1701
Loading
Induction of increased thermotolerance in Saccharomyces cerevisiae may be triggered by a mechanism involving intracellular pH
Microbiology 137, 1701 (1991); https://doi.org/10.1099/00221287-137-7-1701
/content/journal/micro/10.1099/00221287-137-7-1701
/content/journal/micro/10.1099/00221287-137-7-1701
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