Metabolic regulation rather than de novo enzyme synthesis dominates the osmo-adaptation of yeast

Yeast

Volumn 28, Issue 1, 2011, Pages 43-53

  Bouwman, Jildau ^a   Kiewiet, José ^a   Lindenbergh, Alexander ^a   Van Eunen, Karen ^a   Siderius, Marco ^a   Bakker, Barbara M ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Gene expression; Metabolic regulation; Osmotic stress; Regulation analysis; Saccharomyces cerevisiae

Indexed keywords

GLUCOSE; GLYCEROL; MESSENGER RNA; SORBITOL;

ADAPTATION; ARTICLE; ENZYME SYNTHESIS; GENE EXPRESSION; HYPEROSMOTIC STRESS; METABOLIC REGULATION; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; WILD TYPE; YEAST;

ADAPTATION, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, FUNGAL; GLYCEROL; OSMOTIC PRESSURE; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

SACCHAROMYCES CEREVISIAE;

EID: 78650441706     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1819     Document Type: Article

References (48)

1. Albertyn J, Hohmann S, Thevelein JM, Prior BA. 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14: 4135-4144.
2. Ames BN. 1966. Assay of inorganic phosphate, total phosphate and phosphates. Meth Enzymol 8: 115-118.
3. Bakker BM, Overkamp KM, van Maris AJ, et al. 2001. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 15-37.
4. Blomberg A, Adler L. 1989. Roles of glycerol and glycerol-3-phosphate dehydrogenase (NAD+) in acquired osmotolerance of Saccharomyces cerevisiae. J Bacteriol 171: 1087-1092.
5. Brewster JL, Gustin MC. 1994. Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway. Yeast 10: 425-439.
6. Bruggeman FJ, de Haan J, Hardin H, et al. 2006. Time-dependent hierarchical regulation analysis: deciphering cellular adaptation. Syst Biol (Stevenage) 153: 318-322.
7. Canelas AB, van Gulik WM, Heijnen JJ. 2008. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steady-state and highly dynamic conditions. Biotechnol Bioeng 100: 734-743.
8. Capaldi AP, Kaplan T, Liu Y, et al. 2008. Structure and function of a transcriptional network activated by the MAPK Hog1. Nat Genet 40: 1300-1306.
9. Chen RE, Thorner J. 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773: 1311-1340.
10. Cronwright GR, Rohwer JM, Prior BA. 2002. Metabolic control analysis of glycerol synthesis in Saccharomyces cerevisiae. Appl Environ Microbiol 68: 4448-4456.
11. Daran-Lapujade P, Rossell S, van Gulik WM, et al. 2007. The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proc Natl Acad Sci USA 104: 15753-15758.
12. Erasmus DJ, van der Merwe GK, van Vuuren HJ. 2003. Genome-wide expression analyses: Metabolic adaptation of Saccharomyces cerevisiae to high sugar stress. FEMS Yeast Res 3: 375-399.
13. Fell D. 1996. Understanding the Control of Metabolism (Frontiers in Metabolism). Ashgate: Aldershot.
14. Garcia-Martinez J, Aranda A, Perez-Ortin JE. 2004. Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol Cell 15: 303-313.
15. Greatrix BW, van Vuuren HJ. 2006. Expression of the HXT13, HXT15 and HXT17 genes in Saccharomyces cerevisiae and stabilization of the HXT1 gene transcript by sugar-induced osmotic stress. Curr Genet 49: 205-217.
16. Hohmann S, Krantz M, Nordlander B. 2007. Yeast osmoregulation. Meth Enzymol 428: 29-45.
17. Jung S, Marelli M, Rachubinski RA, Goodlett DR, Aitchison JD. 2010. Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress. J Biol Chem 285: 6739-6749.
18. Klipp E, Nordlander B, Kruger R, Gennemark P, Hohmann S. 2005. Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23: 975-82.
19. Kresnowati MT, van Winden WA, Almering MJ, et al. 2006. When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol Syst Biol 2: 49.
20. Kuhn KM, DeRisi JL, Brown PO, Sarnow P. 2001. Global and specific translational regulation in the genomic response of Saccharomyces cerevisiae to a rapid transfer from a fermentable to a nonfermentable carbon source. Mol Cell Biol 21: 916-927.
21. Luyten K, Albertyn J, Skibbe WF, et al. 1995. Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. Embo J 14: 1360-1371.
22. Maeda T, Takekawa M, Saito H. 1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269: 554-558.
23. Mao L, Hartl D, Nolden T, et al. 2008. Pronounced alterations of cellular metabolism and structure due to hyper- or hypo-osmosis. J Proteome Res 7: 3968-3983.
24. Marks VD, Ho Sui SJ, Erasmus D, et al. 2008. Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8: 35-52.
25. Mathai JC, Sauna ZE, John O, Sitaramam V. 1993. Rate-limiting step in electron transport. Osmotically sensitive diffusion of quinones through voids in the bilayer. J Biol Chem 268: 15442-15454.
26. Mettetal JT, Muzzey D, Gomez-Uribe C, van Oudenaarden A. 2008. The frequency dependence of osmo-adaptation in Saccharomyces cerevisiae. Science 319: 482-484.
27. Molin C, Jauhiainen A, Warringer J, Nerman O, Sunnerhagen P. 2009. mRNA stability changes precede changes in steady-state mRNA amounts during hyperosmotic stress. Rna 15: 600-614.
28. Pahlman AK, Granath K, Ansell R, Hohmann S, Adler L. 2001. The yeast glycerol 3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J Biol Chem 276: 3555-3563.
29. Piper MD, Daran-Lapujade P, Bro C, et al. 2002. Reproducibility of oligonucleotide microarray transcriptome analyses. An interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae. J Biol Chem 277: 37001-37008.
30. Posas F, Witten EA, Saito H. 1998. Requirement of STE50 for osmostress-induced activation of the STE11 mitogen-activated protein kinase kinase kinase in the high-osmolarity glycerol response pathway. Mol Cell Biol 18: 5788-5796.
31. Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Arino J. 2000. The transcriptional response of yeast to saline stress. J Biol Chem 275: 17249-17255.
32. Postma E, Scheffers WA, van Dijken JP. 1989. Kinetics of growth and glucose transport in glucose-limited chemostat cultures of Saccharomyces cerevisiae CBS 8066. Yeast 5: 159-165.
33. Ralser M, Wamelink MM, Kowald A, et al. 2007. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol 6: 10.
34. Reed RH, Chudek JA, Foster R, Gadd GM. 1987. Osmotic significance of glycerol accumulation in exponentially growing yeasts. Appl Environ Microbiol 53: 2119-2123.
35. Reiser V, Ruis H, Ammerer G. 1999. Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 1147-1161.
36. Rossell S, van der Weijden CC, Kruckeberg AL, Bakker BM, Westerhoff HV. 2005. Hierarchical and metabolic regulation of glucose influx in starved Saccharomyces cerevisiae. FEMS Yeast Res 5: 611-619.
37. Schmitt ME, Brown TA, Trumpower BL. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucl Acids Res 18: 3091-3092.
38. Siderius M, van Wuytswinkel O, Reijenga KA, Kelders M, Mager WH. 2000. The control of intracellular glycerol in Saccharomyces cerevisiae influences osmotic stress response and resistance to increased temperature. Mol Microbiol 36: 1381-1390.
39. Sussman I, Avron A. 1981. Characterization and partial purification of DL-glycerol-1-phophatase from Dunaliella salina. Biochim Biophys Acta 661: 119-204.
40. Tatebayashi K, Tanaka K, Yang HY, et al. 2007. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. Embo J 26: 3521-3533.
41. ter Kuile BH, Westerhoff HV. 2001. Transcriptome meets metabolome: hierarchical and metabolic regulation of the glycolytic pathway. FEBS Lett 500: 169-171.
42. Vabulas RM, Hartl FU. 2005. Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310: 1960-1963.
43. Valadi A, Granath K, Gustafsson L, Adler L. 2004. Distinct intracellular localization of Gpd1p and Gpd2p, the two yeast isoforms of NAD + -dependent glycerol-3-phosphate dehydrogenase, explains their different contributions to redox-driven glycerol production. J Biol Chem 279: 39677-39685.
44. van Eunen K, Bouwman J, Lindenbergh A, Westerhoff HV, Bakker BM. 2009. Time-dependent regulation analysis dissects shifts between metabolic and gene-expression regulation during nitrogen starvation in baker's yeast. Febs J 276: 5521-5536.
45. van Hoek P, van Dijken JP, Pronk, JT. 1998. Effect of specific growth rate on fermentative capacity of baker's yeast. Appl Environ Microbiol 64: 4226-4233.
46. Verduyn C, Postma E, Scheffers WA, van Dijken JP. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8: 501-517.
47. Westfall PJ, Patterson JC, Chen RE, Thorner J. 2008. Stress resistance and signal fidelity independent of nuclear MAPK function. Proc Natl Acad Sci USA 105: 12212-12217.
48. Wieland OH. 1984. Glycerol: UV-method. Verlag-Chemie: Weinheim.