Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: Variations of PKA effect during stress and growth

Molecular Microbiology

Volumn 35, Issue 2, 2000, Pages 397-406

  Zähringer, Harald ^a   Thevelein, Johan M ^b   Nwaka, Solomon ^a,c,d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c NATL INST BIOSCI HUM TECHNOL   (Japan)

^d QuantaNova Canada Ltd   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL ENZYME; SODIUM CHLORIDE; TRANSCRIPTION FACTOR; TREHALASE; TREHALOSE;

ARTICLE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INDUCTION; ENZYME METABOLISM; ENZYME SYNTHESIS; FUNGUS GROWTH; GENE EXPRESSION REGULATION; GENE FUNCTION; HEAT STRESS; HYDROLYSIS; NONHUMAN; NORTHERN BLOTTING; NUTRIENT; OSMOTIC STRESS; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS;

BASE SEQUENCE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; ENZYME INDUCTION; GENE EXPRESSION REGULATION, FUNGAL; HEAT; LAC OPERON; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OSMOTIC PRESSURE; OXIDATIVE STRESS; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMATION, GENETIC; TREHALASE; TREHALOSE;

EID: 0033959218     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01706.x     Document Type: Article

References (61)

1. App, H., and Holzer, H. (1989) Purification and characterisation of neutral trehalase from yeast ABYS1 mutant. J Biol Chem 263: 17583-17588.
2. Bell, W., Klaassen, P., Ohnacker, M., Boller, T., Herweijer, M., Schoppink, P., et al. (1992) Characterization of the 56kDa subunit of the 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.
3. Bell, W., Sun, W., Hohmann, S., Wera, S., Reinders, A., De Virgilio, C., et al. (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273: 33311 -33319.
4. Blomberg, A., and Adler, L. (1992) Physiology of osmotolerance in fungi. Adv Microbiol Phys 33: 145-212.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
6. De Virgilio, C., Bürckert, N., Boller, T., and Wiemken, A. (1991) A method to study the rapid phosphorylation-related modulation of neutral trehalase activity by temperature shifts in yeast. FEBS Lett 291: 355-358.
7. De Virgilio, C., Bürckert, N., Bell, W., Jeno, P., Boller, T., and Wiemken, A. (1993) Disruption of TPS2, the gene encoding the 100kDa-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.
8. 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.
9. DeRisi, J.L., Iyer, V.R., and Brown, P.O. (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680-686.
10. Elder, R.T., Loy, E.Y., and Davis, R.W. (1983) RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci USA 8: 2432-3436.
11. Fernandez, J., Soto, T., Vicente-Soler, J., Cansado, J., and Gacto, M. (1997) Osmo-stress induced changes in neutral trehalase activity in the fission yeast Schizosaccharomyces pombe. Biochim Biophys Acta 1357: 41-48.
12. Gallwitz, D., and Sures, I. (1980) Structure of a split yeast gene: complete nucleotide sequence of the actin gene in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 77: 2546-2550.
13. Garcia, J.M., Rios, G., Ali, R., Belles, J.M., and Serrano, R. (1997) Comparative physiology of salt tolerance in Candida tropicalis and Saccharomyces cerevisiae. Microbiology 143: 1125-1131.
14. Gietz, R.D., and Schiestl, R.H. (1995) Transforming yeast with DNA. Methods Mol Cell Biol 5: 255-269.
15. 2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12: 586-597.
16. Gounalaki, N., and Thireos, G. (1994) Yap1, a yeast transcriptional activator that mediates multidrug resistance, regulates the metabolic stress response. EMBO J 13: 4036-4041.
17. Herrick, D., Parker, R., and Jacobson, A. (1990) Identification and comparison of stable and unstable mRNAs in S. cerevisiae. Mol Cell Biol 10: 2269-2284.
18. Kienle, I., Burgert, M., and Holzer, H. (1993) Assay of trehalose with acid trehalase purified from Saccharomyces cerevisiae. Yeast 9: 607-611.
19. Kobayashi, N., and McEntee, K. (1993) Identification of cis and trans components of a novel heat shock regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13: 248-256.
20. Kopp, M., Müller, H., and Holzer, H. (1993) Molecular analysis of the neutral trehalase gene from Saccharomyces cerevisiae. J Biol Chem 268: 4766-4774.
21. Kopp, M., Nwaka, S., and Holzer, H. (1994) Corrected sequence of the neutral trehalase encoding gene NTH1: biological implications. Gene 150: 403-404.
22. Lewis, J.G., Learmonth, R.P., and Watson, K. (1995) Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology 141: 687-694.
23. Marchler, G., Schuller, 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.
24. Marquez, J.A., Pascual-Ahuir, A., Proft, M., and Serrano, R. (1998) The Ssn6-Tup1 repressor complex of Saccharomyces cerevisiae is involved in the osmotic induction of HOG-dependent and -independent genes. EMBO J 17: 2543-2553.
25. Martinez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H., and Estruch, F. (1996) The Saccharomyces cerevisiae zinc finger protein Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227-2235.
26. Mazon, M.J., Behrens, M.M., Morgado, E., and Portilo, F. (1993) Low activity of the yeast cAMP-dependent protein kinase catalytic subunit Tpk3 due to the poor expression of the TPK3 gene. Eur J Biochem 213: 501 -506.
27. Mesquita, J.F., Paschoalin, V.M.F., and Panek, A.D. (1997) Modulation of trehalase activity in Saccharomyces cerevisiae by an intrinsic protein. Biochim Biophys Acta 1334: 233-239.
28. Mikaelian, I., and Sergeant, A. (1992) A general and fast method to generate multiple site directed mutations. Nucleic Acids Res 20: 376.
29. Moskvina, E., Schüller, C., Maurer, C.T.C., Mager, W.H., and Ruis, H. (1998) A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast 14: 1041-1050.
30. Myers, A.M., Tzagoloff, A., Kinney, D.M., and Lusty, C. (1986) Yeast shuttle and integrative vectors with multiple cloning sites suitable for construction of lacZ fusions. Gene 45: 299-310.
31. Nikawa, J., Cameron, S., Toda, T., Ferguson, K.W., and Wigler, M. (1987) Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae. Genes Dev 1: 931-937.
32. Nwaka, S., Kopp, M., and Holzer, H. (1995a) Expression and function of the trehalase genes NTH1 and YBR106 in Saccharomyces cerevisiae. J Biol Chem 270: 10193-10198.
33. Nwaka, S., Mechler, B., Destruelle, M., and Holzer, H. (1995b) Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Lett 360: 286-290.
34. Nwaka, S., and Holzer, H. (1998) Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. In Progress in Nucleic Acid Research and Molecular Biology, vol. 58. Moldave, K. (ed.). San Diego: Academic Press, pp. 197-237.
35. Parrou, J.L., Teste, M.-A., and Francois, J. (1997) Effects of various types of stress on the metabolism of reserve carbohydrate in Saccharomyces cerevisiae: genetic evidence for stress-induced recycling of glycogen and trehalose. Microbiology 143: 1891-1900.
36. Parrou, J.L., Enjalbert, B., Plourde, L, Bauche, A., Gonzales, B., and Francois, J. (1999) Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast 15: 191-203.
37. Piper, P.W. (1993) Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 11: 339-356.
38. Piper, P.W. (1998) Differential role of Hsps and trehalose in stress tolerance. Trends Microbiol 6: 43-44.
39. Praekelt, U.M., and Meacock, P.A. (1990) HSP12, a new small heat shock gene of Saccharomyces cerevisiae. Analysis of structure, regulation and function. Mol Gen Genet 223: 97-106.
40. Rose, M.D., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
41. Rothstein, R.J. (1991) Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol 194: 202-211.
42. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A laboratory Manual. Cold Spring Harbor Laboratory Press, NY: Cold Spring Harbor Laboratory Press.
43. San Miguel, P.F., and Arguelles, J.C. (1994) Differential changes in the activity of cytosolic and vacuolar trehalases along the growth cycle of Saccharomyces cerevisiae. Biochim Biophys Acta 1200: 155-160.
44. Schmitt, A.P., and McEntee, K. (1996) Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93: 5777-5782.
45. Sherman, F. (1991) Getting started with yeast. Methods Enzymol 94: 3-21.
46. Siderius, M., and Mager, W.H. (1997) General stress response: in search of a common denominator. In Yeast Stress Responses. Hohmann, S., and Mager, W.H. (eds). Heidelberg: Springer-Verlag, pp. 213-230.
47. Singer, M., and Lindquist, S. (1998) Multiple effects of trehalose on protein folding in-vitro and in-vivo. Mol Cell 1: 639-648.
48. Soto, T., Fernandez, J., Dominguez, A., Vicente-Soler, J., Cansado, J., and Gacto, M. (1998) Analysis of the ntp1' gene, encoding neutral trehalase in the fission yeast Schizosaccharomyces pombe. Biochim Biophys Acta 1443: 225-229.
49. Thevelein, J.M. (1984) Regulation of trehalose mobilization in fungi. Microbiol Rev 48: 42-59.
50. Thevelein, J.M. (1988) Regulation of trehalase activity by phosphorylation-dephosphorylation during developmental transition in fungi. Exp Mycol 12: 1-7.
51. Thevelein, J.M. (1996) Regulation of trehalose metabolism and its relevance to cell growth and function. In The Mycota III, Biochemistry and Molecular Biology. Brambl, R., and Marzluf, G.A. (eds). Heidelberg: Springer-Verlag, pp. 395-414.
52. Thevelein, J.M., and Beullens, M. (1985) Cyclic AMP and the stimulation of trehalase activity in the yeast Saccharomyces cerevisiae by carbon sources, nitrogen sources and inhibitors of protein synthesis. J Gen Microbiol 131: 3199-3209.
53. Toda, T., Cameron, S., Sass, P., Zoller, M., and Wigler, M. (1987) Three different genes in Saccharomyces cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 50: 277-287.
54. Uno, I., Matsumoto, K., Adachi, K., and Ishikawa, T. (1983) Genetic and biochemical evidence that trehalase is a sub-strate of cAMP-dependent protein kinase in yeast. J Biol Chem 258: 10867-10872.
55. Van Dijck, P., Colavizza, D., Smet, P., and Thevelein, J. (1995) Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Appl Environ Microbiol 61: 109-115.
56. Werner, W., Rey, H.-G., and Wielinger, H. (1970) On the properties of a new chromogen for the determination of glucose in blood according to GOD/POD-method. Z Anal Chem 252: 224-226.
57. Wiemken, A. (1990) Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Van Leeuwenhoek 58: 209-217.
58. 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 transcriptional control? Mol Gen Genet 252: 470-482.
59. Zähringer, H. (1999) Regulation und funktion der neutralen trehalase bei der reaktion der hefe Saccaromyces cerevisiae auf globalen stress. PhD thesis. Freiburg, Germany: University of Freiburg.
60. Zähringer, H., Burgert, M., Holzer, H., and Nwaka, S. (1997) Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS Lett 412: 615-620.
61. Zähringer, H., Holzer, H., and Nwaka, S. (1998) Stability of neutral trehalase during heat stress in Saccharomyces cerevisiae is dependent on the catalytic subunits of cAMP-dependent protein kinase, Tpk1 and Tpk2. Eur J Biochem 255: 544-551.