Synergy between trehalose and Hsp104 for thermotolerance in Saccharomyces cerevisiae

Genetics

Volumn 144, Issue 3, 1996, Pages 923-933

  Elliott, Beth ^a,b   Haltiwanger, Robert S ^b   Futcher, Bruce ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; TREHALOSE;

ARTICLE; CELL CYCLE S PHASE; ENZYME ACTIVE SITE; FUNGUS GROWTH; FUNGUS MUTANT; FUNGUS MUTATION; GENE LOCUS; GROWTH REGULATION; HEAT TOLERANCE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; FUNGAL PROTEINS; HEAT-SHOCK PROTEINS; HEATING; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC; TREHALOSE;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0029861940     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. ALDRIDGE, S., 1995 Trehalose boosts prospects for improved biopharmaCeuticals and vaccines. Genet. Eng. News 15: 10-11.
2. BARNES, C. A., G. C. JOHNSTON and R. A. SINGER, 1990 Thermotolerance is independent of induction of the full spectrum of heat shock proteins and of cell cycle blockage in the yeast Saccharomyces cerevisiae. J. Bacteriol. 172: 4352-4358.
3. BELL, W., P. KLAASSEN, M. OHNACKER, T. BOLLER, M. HERW-EIJER et al., 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.
4. BENNETZEN, J. L., and B. D. HALL, 1982 Codon selection in yeast. J. Biol. Chem. 257: 3026-3031.
5. BLÁZQUEZ, M. A., R. LACUNAS, C. GANCEDO andj. M. GANCEDO, 1993 Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEES Lett. 329: 51-54.
6. BROACH, J. R., and R. J. DESCHENES, 1990 The function of RAS genes in Saccharomyces cerevisiae. Adv. Cancer Res. 54: 79-139.
7. CABIB, E., and F. L. LELOIR, 1958 The biosynthesis of trehalose-6-phosphate. J. Biol. Chem. 231: 259-275.
8. CAMERON, S., L. LEVIN, M. ZOLLER and M. WIGLER, 1988 cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell 52: 555-566.
9. COLAçO, C., S. SEN, M. THANGAVELU, S. FINDER and R. ROSER, 1992 Extraordinary stability of enzymes dried in trehalose: simplified molecular biology. Biotechnology 10: 1007-1011.
10. CRO\VE, J. H., L. M. CROWE and D. CHAPMAN, 1984 Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223: 701-703.
11. DE VIRGIUO, C., U. SIMMEN, T. HOTTIGER, T. BOH.ER and A. WIEMKEN, 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.
12. DE VIRGILIo, C., P. PIPER, T. BOLLER and A. WIEMKEN, 1991 Acquisition of thermotolerance in Saccharomyces cerevisiae without heat shock protein hsp104 and in the absence of protein synthesis. FEBS Lett. 288: 355-358.
13. DE VIRGIUO, C., N. BURCKERT, W. BELL, P. JENO, T. BOLLER et ai, 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: 315-323.
14. DE VIRGILIO, C., T. HOTTIGER, J. DOMINGUEZ, T. BOLLER and A. WIEMKEN, 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.
15. DUJON, B., D. ALEXANDRAKI, B. ANDRE, W. ANSORGE, V. BALADRON et al, 1994 Complete DNA sequence of yeast chromosome XI. Nature 369: 371-378.
16. ELBIEN, A. D., 1974 The metabolism of α-α trehalose. Adv. Carbohydr. Chem. Biochem. 30: 227-256.
17. HEINISCH, J., R. C. Vox BORSTEL and R. RODICO, 1991 Sequence and localization of the gene encoding yeast phosphoglycerate mutase. Curr. Genet. 20: 167-171.
18. HENGGE-ARONIS, R., Vf. KLEIN, R. LANGE, M. RIMMELE and W. Boos, 1991 Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationaryphase thermotolerance in Escherichia coll. J. Bacteriol. 173: 7918-7924.
19. HOHMANN, S., M. J. NEVES, W. DE KONING, R. ALIJO, J. RAMOS et al., 1993 The growth and signalling defects of the ggsl (fdpl/ bypl) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PH. Curr. Genet. 23: 281-289.
20. HOTTIGER, T., T. BOLLER and A. WIEMKEN, 1987 Rapid changes of heat and desiccation tolerance correlated with" changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett. 220: 113-115.
21. HOTTIGER, T., T. BOLLER and A. WIEMKEN, 1989 Correlation of 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. HOTTIGER, T., C. DE VIRGILIO, W. BELL, T. BOLLER and A. WIEMKEN, 1992 The 70-kilodalton heat-shock proteins of the SSA subfamily negatively modulate heat-shock-induced accumulation of trehalose and promote recovery from heat stress in the yeast Saccharomyces cerevisiae. Eur.J. Biochem. 210: 125-132.
23. HOTTIGER, T., C. DE VIRGILIO, M. N. HALL, T. BOLLER and A. WIEMKEN, 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. JOULIN, V., M.-C. GAREL, P. LE BOULCH, C. VALENTIN, R. Rosa et al, 1988 Isolation and characterization of the human 2,3-bisphosphoglycerate mutase gene. J. Biol. Chem. 262: 15785-15790.
25. KILLICK, K. A., and B. E. WRIGHT, 1972 Trehalose synthesis during differentiation in Dictyostelium discoideum. 3. In vitro unmasking of trehalose-6-phosphatase synthetase. J. Biol. Chem. 247: 2967-2969.
26. KLECKNER, N., J. BENDER and S. GOTTESMAN, 1991 Uses of transposons with emphasis on TnlO. Methods Enzymol. 204: 139-179.
27. LILUE, S. H., andj. R. PRINGLE, 1980 Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143: 1384-1394.
28. LINDQUIST, S. L., and E. A. CRAIG, 1988 The heat shock proteins. Annu. Rev. Genet. 22: 631-677.
29. NEVES, M.-J., and J. FRANçOIS, 1992 On the mechanism by which a heat shock induces trehalose accumulation in Saccharomyces cerevisiae. J. Biochem. 288: 859-864.
30. NEVES, M.-J., J. A. JORGE, J. M. FRANÇOIS and H. F. TERENZI, 1991 Effects of heat shock on the level of trehalose and glycogen, and the induction of thermotolerance in Neurospora crassa. FEBS Lett. 283: 19-22.
31. OLSON, M. V., J. E. DUTCHIK, M. Y. GRAILVM, G. M. BRODEUR, C. M. HELMS et al., 1986 Random-clone strategy for genomic restriction mapping in yeast. Proc. Natl. Acad. Sei. USA 83: 7826-7830.
32. PARSELL, D. A., A. S. KOWAL, M. A. SINGER and S. LINDQUIST, 1994 Protein disaggregation mediated by heat shock protein Hspl04. Nature 372: 475-478.
33. PILKIS, S. J., M. O. LIVELY and M. R. EL-MAGIIRABI, 1987 Active site sequence of hepatic fructose-2,6-bisphosphatasc. J. Biol. Chem. 262: 12672-12675.
34. PIPER, P. W., and A. LOCKHEART, 1988 A temperature-sensitive mutant of Saccharomyces cerevisiae defective in the specific phosphatase of trehalose biosynthesis. FEMS Microbiol. Lett. 49: 245-250.
35. PRINGLE,J. R., and L. H. HARWELL, 1981 The Saccharomyces cerevisiae cell cycle, pp. 97-142 in The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance, edited byj. N. STRATI IERN, E. W. JONES andj. R. BROACH. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. SAMBROOK, J., E. F. FRITSCII and T. MANLYTIS, 1989 Molecular Cloning: A Laboratory Manual. Co'ld Spring Harbor Laboratory Press, Cold Spring Harbor, NY. .
37. SANCHEZ, Y., and S. LINDQUIST, 1990 HSP104 required for induced thermotolerance. Science 248: 1112-1115.
38. SANCHEZ, Y., J. TAUI.IEN, K. A. BORKOVICH and S. LINDQUIST, 1992 Hspl04 is required for tolerance to many forms of stress. EMBO J. 11: 2357-2364.
39. SANGER, F., S. NICKI.EN and A. R. COUI.SON, 1977 DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sei. USA 74: 5463-5467.
40. SCIIENBERG-FRASCINO, A., and E. MOUSTACCHI, 1972 Lethal and inutagenic effects of elevated temperature on haploid yeast. Mol. Gen. Genet. 115:243-257.
41. SCHULZE, C., 1895 Dieanwendungdcspasteurisirensgegennachgahrungcn der weine auf den flaschen. Landwirtsch. Jahrb. 24:403-433.
42. SIIER.\L\N, F., 1956 The heat inaclivation and production of cytochrome deficiency in yeast. Exp. Cell Res. 11: 659-660.
43. SIIERMAN, F., G. R. FINK andj. B. HICKS, 1986 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. SMITH, B. J., and M. P. YAFFE, 1991 Uncoupling thermotolerance from the induction of heat shock proteins. Proc. Natl. Acad. Sei. USA 88: 11091-11094.
45. SUR, I. P., Z. LOBO and P. K. MAITRA, 1994 Analysis of PFK3 - a gene involved in paniculate phosphofructokinase synthesis reveals additional functions of 7PS2 in Saccharomyces cerevisiae. Yeast 10: 199-209.
46. THEVEI.EIN.J. M., and S. HOHMANN, 1995 Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochcm. Sei. 20: 3-10.
47. TODA, T., S. CAMERON, P. SASS, M. ZOI.I.ER and M. WIGI.ER, 1987 Three different genes in S. cerevisiae encode the catalytic subunit of cAMP-dependent protein kinase. Cell 50: 277-287.
48. TOKIWA, G., M. TVERS, T. VOI.PF. and B. FUTCIIF.R, 1994 Inhibition of Gl cyclin activity by the RAS/cAMP pathway in yeast. Nature 371: 342-345.
49. VUORIO, O-, N. KAI.KKINEN and J. LONDESBOROUGII, 1993 Cloning of two related genes encoding the 56 kDa and 123 kDa subunits of trehalosc synthase from the yeast Saccharomyces cerevisiae. Eur. J. Biochcm. 216: 849-861.
50. WERNER-WASIIBURNE, M., D. E. STONE and E. A. CRAIG, 1987 Complex interactions among members of an essential subfamily of Hsp70 genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 2568-2577.
51. WHITE, P. J..J. NAIRN, N. C. PRICE, H. G. NIMMO, J. R. COGGINS et al, 1992 Phosphoglycerate mutase from Streptomyces coclicolor A3(2): purification and characterization of the enzyme and cloning and sequence analysis of the gene. J. Bacteriol. 174: 434-440.