Quantitative Analysis of Glycerol Accumulation, Glycolysis and Growth under Hyper Osmotic Stress

PLoS Computational Biology

Volumn 9, Issue 6, 2013, Pages

  Petelenz Kurdziel, Elzbieta ^a,e   Kuehn, Clemens ^b   Nordlander, Bodil ^a   Klein, Dagmara ^a,f   Hong, Kuk Ki ^c   Jacobson, Therese ^a   Dahl, Peter ^a   Schaber, Jörg ^b,d   Nielsen, Jens ^c   Hohmann, Stefan ^a   Klipp, Edda ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b HUMBOLDT UNIVERSITY   (Germany)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^d UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

^e UNIVERSITY OF BERGEN   (Norway)

^f Thermo Fisher Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGY; ENZYMES; GENE EXPRESSION REGULATION; METABOLISM; OSMOSIS; PATHOLOGY; SODIUM CHLORIDE; TRANSCRIPTION; YEAST;

CELLULAR ACTIVITIES; EUKARYOTICS; GENES EXPRESSION; GLYCEROL PRODUCTION; GLYCOLYTIC FLUX; HYPER-OSMOTIC SHOCK; METABOLIC CONTROL; OSMO-ADAPTATION; OSMOLYTES; OSMOTIC STRESS;

GLYCEROL;

CARRIER PROTEIN; GLYCEROL; PHOSPHOTRANSFERASE; PROTEIN HOG1; PROTEIN PFK26; PROTEIN PFK27; PROTEIN STL1; TREHALOSE; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; BIOMASS; CELL GROWTH; FUNGAL BIOMASS; FUNGAL CELL; GLYCOLYSIS; GROWTH INHIBITION; HYPEROSMOTIC STRESS; LIPID STORAGE; LIPOGENESIS; MATHEMATICAL MODEL; MUTANT; NONHUMAN; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE; SALT STRESS; UPREGULATION; WILD TYPE;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84879517894     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003084     Document Type: Article

References (47)

1. Yancey PH, (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208: 2819-2830.
2. Klipp E, Nordlander B, Kruger R, Gennemark P, Hohmann S, (2005) Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23: 975-982.
3. Mettetal JT, Muzzey D, Gomez-Uribe C, van Oudenaarden A, (2008) The frequency dependence of osmo-adaptation in Saccharomyces cerevisiae. Science 319: 482-484.
4. Zi Z, Liebermeister W, Klipp E, (2010) A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. PLoS One 5: e9522.
5. Schaber J, Baltanas R, Bush A, Klipp E, Colman-Lerner A, (2012) Modelling reveals novel roles of two parallel signalling pathways and homeostatic feedbacks in yeast. Mol Syst Biol 8: 622.
6. Ansell R, Granath K, Hohmann S, Thevelein JM, Adler L, (1997) The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16: 2179-2187.
7. Luyten K, Albertyn J, Skibbe WF, Prior BA, Ramos J, 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.
8. Tamas MJ, Luyten K, Sutherland FC, Hernandez A, Albertyn J, et al. (1999) Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol Microbiol 31: 1087-1104.
9. Albertyn J, Hohmann S, Prior BA, (1994) Characterization of the osmotic-stress response in Saccharomyces cerevisiae: osmotic stress and glucose repression regulate glycerol-3-phosphate dehydrogenase independently. Curr Genet 25: 12-18.
10. Påhlman 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.
11. 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.
12. 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.
13. Rep M, Albertyn J, Thevelein JM, Prior BA, Hohmann S, (1999) Different signalling pathways contribute to the control of GPD1 gene expression by osmotic stress in Saccharomyces cerevisiae. Microbiology 145 (Pt 3):: 715-727.
14. Norbeck J, Påhlman AK, Akhtar N, Blomberg A, Adler L, (1996) Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. Identification of the corresponding GPP1 and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway. J Biol Chem 271: 13875-13881.
15. Hirayama T, Maeda T, Saito H, Shinozaki K, (1995) Cloning and characterization of seven cDNAs for hyperosmolarity-responsive (HOR) genes of Saccharomyces cerevisiae. Mol Gen Genet 249: 127-138.
16. Remize F, Barnavon L, Dequin S, (2001) Glycerol export and glycerol-3-phosphate dehydrogenase, but not glycerol phosphatase, are rate limiting for glycerol production in Saccharomyces cerevisiae. Metab Eng 3: 301-312.
17. Dihazi H, Kessler R, Eschrich K, (2004) High osmolarity glycerol (HOG) pathway-induced phosphorylation and activation of 6-phosphofructo-2-kinase are essential for glycerol accumulation and yeast cell proliferation under hyperosmotic stress. J Biol Chem 279: 23961-23968.
18. Tamas MJ, Karlgren S, Bill RM, Hedfalk K, Allegri L, et al. (2003) A short regulatory domain restricts glycerol transport through yeast Fps1p. J Biol Chem 278: 6337-6345.
19. Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, et al. (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol Biol Cell 16: 2068-2076.
20. Rep M, Krantz M, Thevelein JM, Hohmann S, (2000) The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275: 8290-8300.
21. Westfall PJ, Patterson JC, Chen RE, Thorner J, (2008) Stress resistance and signal fidelity independent of nuclear MAPK function. Proc Natl Acad Sci U S A 105: 12212-12217.
22. Kuhn C, Petelenz E, Nordlander B, Schaber J, Hohmann S, et al. (2008) Exploring the impact of osmoadaptation on glycolysis using time-varying response-coefficients. Genome Inform 20: 77-90.
23. Schaber J, Klipp E, (2008) Short-term volume and turgor regulation in yeast. Essays Biochem 45: 147-159 doi: 10.1042/BSE0450147.
24. Schaber J, Adrover MA, Eriksson E, Pelet S, Petelenz-Kurdziel E, et al. (2010) Biophysical properties of Saccharomyces cerevisiae and their relationship with HOG pathway activation. Eur Biophys J 39: 1547-1556.
25. Teusink B, Passarge J, Reijenga CA, Esgalhado E, van der Weijden CC, et al. (2000) Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 267: 5313-5329.
26. Clotet J, Escote X, Adrover MA, Yaakov G, Gari E, et al. (2006) Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. Embo J 25: 2338-2346.
27. Escote X, Zapater M, Clotet J, Posas F, (2004) Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6: 997-1002.
28. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
29. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, et al. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323-337.
30. Nordlander B, Krantz M, Hohmann S (2008) Hog1-mediated Metabolic Adjustments Following Hyperosmotic Shock in the Yeast Saccharomyces cerevisiae. In: Posas F, Nebreda AR, editors. Stress-Activated Protein Kinases. Berlin/Heidelberg: Springer. pp. 141-158.
31. Rep M, Reiser V, Gartner U, Thevelein JM, Hohmann S, et al. (1999) Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msn1p and the novel nuclear factor Hot1p. Mol Cell Biol 19: 5474-5485.
32. Ou X, Ji C, Han X, Zhao X, Li X, et al. (2006) Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1). J Mol Biol 357: 858-869.
33. Muzzey D, Gomez-Uribe CA, Mettetal JT, van Oudenaarden A, (2009) A systems-level analysis of perfect adaptation in yeast osmoregulation. Cell 138: 160-171.
34. Ingalls BP, Sauro HM, (2003) Sensitivity analysis of stoichiometric networks: an extension of metabolic control analysis to non-steady state trajectories. J Theor Biol 222: 23-36.
35. Kuhn C, Klipp E, (2012) Zooming in on yeast osmoadaptation. Adv Exp Med Biol 736: 293-310.
36. Mollapour M, Piper PW, (2007) Hog1 Mitogen-Activated Protein Kinase Phosphorylation Targets the Yeast Fps1 Aquaglyceroporin for Endocytosis, Thereby Rendering Cells Resistant to Acetic Acid. Mol Cell Biol 27: 6446-6456.
37. Thorsen M, Di Y, Tängemo C, Morillas M, Ahmadpour D, et al. (2006) The MAPK Hog1p Modulates Fps1p-dependent Arsenite Uptake and Tolerance in Yeast. Mol Biol Cell 17: 4400-4410.
38. Beese SE, Negishi T, Levin DE, (2009) Identification of positive regulators of the yeast fps1 glycerol channel. PLoS Genet 5: e1000738.
39. Davis DJ, Burlak C, Money NP, (2000) Osmotic pressure of fungal compatible osmolytes. Mycological Research 104: 800-804.
40. Pagnotta SE, McLain SE, Soper AK, Bruni F, Ricci MA, (2010) Water and trehalose: how much do they interact with each other? J Phys Chem B 114 (14):: 4904-4908.
41. Pereira CS, Hunenberger PH, (2008) Effect of trehalose on a phospholipid membrane under mechanical stress. Biophys J 95: 3525-3534.
42. Nordlander B, Krantz M, Hohmann S (2008) Hog1-mediated Metabolic Adjustments Following Hyperosmotic Shock in the Yeast Saccharomyces cerevisiae. Stress-Activated Protein Kinases. Berlin/Heidelberg: Springer pp. 141-158.
43. Bruggeman FJ, de Haan J, Hardin H, Bouwman J, Rossell S, et al. (2006) Time-dependent hierarchical regulation analysis: deciphering cellular adaptation. Syst Biol (Stevenage) 153: 318-322.
44. Duch A, de Nadal E, Posas F, (2012) The p38 and Hog1 SAPKs control cell cycle progression in response to environmental stresses. FEBS Lett 586: 2925-2931.
45. Thomas BJ, Rothstein RJ, (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56: 619-630.
46. Maiwald T, Timmer J, (2008) Dynamical modeling and multi-experiment fitting with PottersWheel. Bioinformatics 24: 2037-2043.
47. Zi Z, Klipp E, (2006) SBML-PET: a Systems Biology Markup Language-based parameter estimation tool. Bioinformatics 22: 2704-2705.