Trehalose synthesis is important for the acquisition of thermotolerance in Schizosaccharomyces pombe

Molecular Microbiology

Volumn 25, Issue 3, 1997, Pages 571-581

  Ribeiro, Maria J S ^a   Reinders, Anke ^a   Boller, Thomas ^a   Wiemken, Andres ^a   De Virgilio, Claudio ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; HEAT SHOCK PROTEIN; TREHALOSE;

ARTICLE; FUNGUS GROWTH; GENOTYPE; HEAT SHOCK; HEAT TOLERANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SCHIZOSACCHAROMYCES POMBE; YEAST;

FUNGI; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 0030868257     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.4961856.x     Document Type: Article

References (53)

1. Ang, D., Liberek, K., Skowyra, D., Zylicz, M., and Georgopoulos, C. (1991) Biological role and regulation of the universally conserved heat shock proteins. J Biol Chem 266: 24233-24236.
2. Attfield, P.V. (1987) Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett 225: 259-263.
3. Beckman, R.P., Mizzen, L.A., and Welch, W.J. (1990) Interaction of Hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science 248: 850-854.
4. Bell, W., Klaassen, P., Ohnacker, M., Boller, T., Herweijer, M., Schoppink, P., Van der Zee, P., and Wiemken, A. (1992) Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 209: 951-959.
5. Blázquez, M.A., Stucka, R., Feldmann, H., and Gancedo, C. (1994) Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. J Bacteriol 176: 3895-3902.
6. Boorstein, W.R., and Craig, E.A. (1990) Regulation of yeast HSP70 gene by a cAMP responsive transcriptional control element. EMBO J 9: 2543-2553.
7. Cheng, M.Y., Hartl, F.-U., Martin, J., Pollock, R.A., Kalousek, F., Neupert, W., Hallberg, E.M., Hallberg, R.L., and Horwich, A.-L. (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337: 620-625.
8. Crowe, J.H., Crowe, L.M., Carpenter, J.F., and Wistrom, C.A. (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242: 1-10.
9. Degols, G., Shiozaki, K., and Russel, P. (1996) Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol Cell Biol 16: 2870-2877.
10. De Virgilio, C., Simmen, U., Hottiger, T., Boller, T., and Wiemken, A. (1990) Heat shock induces enzymes of trehalose metabolism, trehalose accumulation, and thermotolerance in Schizosaccharomyces pombe, even in the presence of cycloheximide. FEBS Lett 273: 107-110.
11. De Virgilio, C., Piper, P., Boller, T., and Wiemken, A. (1991) Acquisition of thermotolerance in Saccharomyces cerevisiae without heat shock protein hsp104 and in the absence of protein synthesis. FEBS Lett 288: 86-90.
12. De Virgilio, C., Bürckert, N., Bell, W., Boller, T., and Wiemken, A. (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212: 315-232.
13. De Virgilio, C., Hottiger, T., Dominguez, J., Boller, T., and Wiemken, A. (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. Eur J Biochem 219: 179-186.
14. + protein kinase and cAMP dependent protein kinase as negative regulators of fission yeast meiosis. EMBO J 10: 3759-3768.
15. Elliott, B., Haltiwanger, R.S., and Futcher, B. (1996) Synergy between tranalose and Hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 144: 923-933.
16. Fernández, T., Soto, T., Vicente-Soler, J., Cansado, J., and Gacto, M. (1997) Heat-shock response in Schizosaccharomyces pombe cells lacking cyclic AMP-dependent phosphorylation. Curr Genet 31: 112-118.
17. Finley, D., Özkaynak, E., and Varshavsky, A. (1987) The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48: 1035-1046.
18. Gething, M.-J., and Sambrook, J. (1992) Protein folding in the cell. Nature 355: 33-45.
19. Gounalaki, N., and Thireos, G. (1994) Yap1p, a yeast transcriptional activator that mediates multidrug resistance, regulates the metabolic stress response. EMBO J 13: 4036-4041.
20. Hottiger, T., Schmutz, P., and Wiemken, A. (1987) Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169: 5518-5522.
21. Hottiger, T., Boller, T., and Wiemken, A. (1989) Correlation between trehalose content and heat resistance in yeast mutants altered in the Ras/adenylate cyclase pathway: is trehalose a thermoprotectant? FEBS Lett 255: 431-434.
22. Hoffman, C.S., and Winston, F. (1991) Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev 5: 561-571.
23. Hottiger, T., De Virgilio, C., Hall, M.N., Boller, T., and Wiemken, A. (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur J Biochem 219: 187-193.
24. 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. Mol Cell Biol 8: 5555-5560.
25. Jakobsen, B.K., and Pelham, H.R.B. (1988) Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol 8: 5040-5042.
26. Jin, M., Fujita, M., Culley, B.M., Apolinario, E., Yamamoto, M., Maundrell, K., and Hoffman, C.S. (1995) sck1, a high copy number suppressor of defects in the cAMP-depen-dent protein kinase pathway in fission yeast, encodes a protein homologous to the Saccharomyces cerevisiae SCH9 kinase. Genetics 140: 457-467.
27. Kang, P.-J., Ostermann, J., Shilling, J., Neupert, W., Craig, E., and Pfanner, N. (1990) Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348: 137-143.
28. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
29. Lindquist, S. (1986) The heat-shock response. Annu Rev Biochem 55: 1151-1191.
30. Londesborough, J., and Varimo, K. (1984) Characterization of two trehalases in baker's yeast. Biochem J 219: 511-518.
31. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
32. Maeda, T., Watanabe, Y., Kunitomo, H., and Yamamoto, M. (1994) Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J Biol Chem 269: 9632-9637.
33. Mager, W.H., and Ferreira, M. (1993) Stress response of yeast. Biochem J 290: 1-13.
34. Marchler, G., Schüller, C., Adam, G., and 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.
35. Mochizuki, N., and Yamamoto, M. (1992) Reduction in the intracellular cAMP level triggers initiation of sexual development in fission yeast. Mol Gen Genet 233: 17-24.
36. Moreno, S., Klar, A., and Nurse, P. (1991) Molecular genetic analysis of the fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.
37. Parsell, D.A., Kowal, A.S., Singer, M.A., and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478.
38. Piper, P.W. (1993) Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 11: 339-356.
39. Reinders, A., Bürckert, N., Hohmann, S., Thevelein, J., Boller, T., Wiemken, A., and De Virgilio, C. (1997) Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Mol Microbiol 24: 687-695.
40. Ribeiro, M.J.S., Silva, J.T., and Panek, A.D. (1994) Trehalose metabolism in Saccharomyces cerevisiae during heat-shock. Biochim Biophys Acta 1200: 139-147.
41. Schüller, C., Brewster, J.L., Alexander, M.R., Gustin, M.C., and Ruis, H. (1994) The HOG pathway controls osmotic regulation of transcription via stress response elements (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J 13: 4382-4389.
42. Shin, D.-Y., Matsumoto, K., Iida, H., Uno, I., and Ishikawa, T. (1987) Heat shock response of Saccharomyces cerevisiae mutants altered in cyclic AMP-dependent protein phosphorylation. Mol Cell Biol 7: 244-250.
43. Sorger, P.K., and Pelham, H.R.B. (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54: 855-864.
44. Soto, T., Fernández, J., Cansado, J., Vicente-Soler, J., and Gacto, M. (1995) Glucose-induced, cyclic-AMP-independent signalling pathway for activation of neutral trehalase in the fission yeast Schizosaccharomyces pombe. Microbiology 141: 2665-2671.
45. Thevelein, J.M. (1992) The RAS-adenylate cyclase pathway and cell cycle control in Saccharomyces cerevisiae. Anton Leeuwenhoek 62: 109-130.
46. Thevelein, J.M., and Hohmann, S. (1995) Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem Sci 20: 3-10.
47. Varela, J.C.S., Praekelt, U.M., Meacock, P.A., Planta, R.J., and 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.
48. Vuorio, O.E., Kalkkinen, N., and Londesborough, J. (1993) Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. Eur J Biochem 261: 848-861.
49. Wiemken, A. (1990) Trehalose in yeast, stress protectant rather than reserve carbohydrate. Anton Leeuwenhoek 58: 209-217.
50. Wieser, R., Adam, G., Wagner, A., Schüller, C., Marchler, G., Ruis, H., Krawiec, Z., and 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.
51. Winderickx, J., de Winde, J.H., Crauwels, M., Hino, A., Hohmann, S., Van Dijck, P., and Thevelein, J.M. (1996) Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Mol Gen Genet 252: 470-482.
52. Yamawaki-Kataoka, Y., Tamaoki, T., Choe, H.-R., Tanaka, H., and Kataoka, T. (1989) Adenylate cyclases in yeast: a comparison of the genes from Schizosaccharomyces pombe and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 86: 5693-5697.
53. Young, D., Riggs, M., Fields, J., Vojtek, A., Broek, D., and Wigler, M. (1989) The adenylyl cyclase gene from Schizosaccharomyces pombe. Proc Natl Acad Sci USA 86: 7989-7993.