A kinetic model of catabolic adaptation and protein reprofiling in Saccharomyces cerevisiae during temperature shifts

FEBS Journal

Volumn 281, Issue 3, 2014, Pages 825-841

  Mensonides, Femke I C ^a   Brul, Stanley ^a   Hellingwerf, Klaas J ^a   Bakker, Barbara M ^b   Teixeira De Mattos, M Joost ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Chemostat; Heat stress; Metabolism; Modelling; Protein turnover

Indexed keywords

GLUCOSE; PROTEOME; TREHALOSE;

ARTICLE; CELL DEATH; CELL VIABILITY; DEGRADATION KINETICS; ENERGY CONSERVATION; ENERGY CONSUMPTION; ENVIRONMENTAL TEMPERATURE; ENZYME SYNTHESIS; FUNGAL BIOMASS; FUNGUS GROWTH; GLUCOSE INTAKE; GROWTH DISORDER; HIGH TEMPERATURE; MATHEMATICAL MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; TEMPERATURE DEPENDENCE;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BATCH CELL CULTURE TECHNIQUES; CELL DEATH; CELL PROLIFERATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HOT TEMPERATURE; KINETICS; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; OXIDATIVE PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TREHALOSE;

EID: 84897878310     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12649     Document Type: Article

References (60)

1. Coote PJ, Cole MB & Jones MV (1991) Induction of increased thermotolerance in Saccharomyces cerevisiae may be triggered by a mechanism involving intracellular pH. J Gen Microbiol 137, 1701-1708.
2. Lloyd D, Morrell S, Carlsen HN, Degn H, James PE & Rowlands CC (1993) Effects of growth with ethanol on fermentation and membrane fluidity of Saccharomyces cerevisiae. Yeast 9, 825-833.
3. Piper PW (1997) The yeast heat stress response. In Yeast Stress Responses (Hohmann S & Mager WH, eds), pp. 75-99. Landes, Austin, TX.
4. Viegas CA, Sebastiao PB, Nunes AG & Sa-Correia I (1995) Activation of plasma membrane H(+)-ATPase and expression of PMA1 and PMA2 genes in Saccharomyces cerevisiae cells grown at supraoptimal temperatures. Appl Environ Microbiol 61, 1904-1909.
5. Attfield PV (1987) Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett 225, 259-263.
6. Attfield PV, Kletsas S & Hazell BW (1994) Concomitant appearance of intrinsic thermotolerance and storage of trehalose in Saccharomyces cerevisiae during early respiratory phase of batch-culture is CIF1-dependent. Microbiology 140, 2625-2632.
7. Boy-Marcotte E, Lagniel G, Perrot M, Bussereau F, Boudsocq A, Jacquet M & Labarre J (1999) The heat shock response in yeast: differential regulations and contributions of the Msn2p/Msn4p and Hsf1p regulons. Mol Microbiol 33, 274-283.
8. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES & Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12, 323-337.
9. Devirgilio C, Hottiger T, Dominguez J, Boller T & Wiemken A (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. 1. Genetic evidence that trehalose is a thermoprotectant. Eur J Biochem 219, 179-186.
10. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D & Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11, 4241-4257.
11. Jenkins GM, Richards A, Wahl T, Mao C, Obeid L & Hannun Y (1997) Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. J Biol Chem 272, 32566-32572.
12. Kamada Y, Jung US, Piotrowski R & Levin DE (1995) The protein kinase C activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9, 1559-1571.
13. Lindquist S & Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22, 631-677.
14. Miller MJ, Xuong NH & Geiduschek EP (1982) Quantitative analysis of the heat shock response of Saccharomyces cerevisiae. J Bacteriol 151, 311-327.
15. Patton JL & Lester RL (1991) The phosphoinositol sphingolipids of Saccharomyces cerevisiae are highly localized in the plasma membrane. J Bacteriol 173, 3101-3108.
16. Piper PW (1993) Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 11, 339-355.
17. Simola M, Hanninen AL, Stranius SM & Makarow M (2000) Trehalose is required for conformational repair of heat-denatured proteins in the yeast endoplasmic reticulum but not for maintenance of membrane traffic functions after severe heat stress. Mol Microbiol 37, 42-53.
18. Thevelein JM (1984) Regulation of trehalose mobilization in fungi. Microb Rev 48, 42-59.
19. Van Uden N (1984) Temperature profiles of yeasts. Adv Microb Physiol 25, 195-251.
20. Mensonides FIC, Schuurmans JM, Teixeira de Mattos MJ, Hellingwerf KJ & Brul S (2002) The metabolic response of Saccharomyces cerevisiae to continuous heat stress. Mol Biol Rep 29, 103-106.
21. Dubois MF, Hovanessian AG & Bensaude O (1991) Heat-shock-induced denaturation of proteins. Characterization of the insolubilization of the interferon-induced p68 kinase. J Biol Chem 266, 9707-9711.
22. Nguyen VT, Morange M & Bensaude O (1989) Protein denaturation during heat shock and related stress. Escherichia coli beta-galactosidase and Photinus pyralis luciferase inactivation in mouse cells. J Biol Chem 264, 10487-10492.
23. Pace B & Campbell LL (1967) Correlation of maximal growth temperature and ribosome heat stability. Proc Natl Acad Sci USA 57, 1110-1116.
24. Teixeira P, Castro H, Mohacsi-Farkas C & Kirby R (1997) Identification of sites of injury in Lactobacillus bulgaricus during heat stress. J Appl Microbiol 83, 219-226.
25. Verduyn C (1991) Physiology of yeasts in relation to biomass yields. Antonie Van Leeuwenhoek 60, 325-353.
26. Forrest WW & Walker DJ (1971) The generation and utilization of energy during growth. Adv Microb Physiol 5, 213-274.
27. Lange HC & Heijnen JJ (2001) Statistical reconciliation of the elemental and molecular biomass composition of Saccharomyces cerevisiae. Biotechnol Bioeng 75, 334-344.
28. Stouthamer AH (1973) A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39, 545-565.
29. Verduyn C, Stouthamer AH, Scheffers WA & van Dijken JP (1991) A theoretical evaluation of growth yields of yeasts. Antonie Van Leeuwenhoek 59, 49-63.
30. Parsell DA & Lindquist S (1993) The function of heatshock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27, 437-496.
31. Singer MA & Lindquist S (1998) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1, 639-648.
32. Hoppe GK & Hansford GS (1982) Ethanol inhibition of continuous anaerobic yeast growth. Biotechol Lett 4, 39-44.
33. Novak M, Strehaiano P, Moreno M & Goma G (1981) Alcoholic fermentation: on the inhibitory effect of ethanol. Biotechnol Bioeng 23, 201-211.
34. Piper PW (1995) The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol Lett 134, 121-127.
35. Zuzuarregui A & del Olmo M (2004) Analyses of stress resistance under laboratory conditions constitute a suitable criterion for wine yeast selection. Antonie Van Leeuwenhoek 85, 271-280.
36. Mensonides FIC, Brul S, Klis FM, Hellingwerf KJ & Teixeira de Mattos MJ (2005) Activation of the protein kinase C1 pathway upon continuous heat stress in Saccharomyces cerevisiae is triggered by an intracellular increase in osmolarity due to trehalose accumulation. Appl Environ Microbiol 71, 4531-4538.
37. Mensonides FIC (2007) How Saccharomyces cerevisiae copes with heat stress-an experimental and theoretical study. PhD thesis, University of Amsterdam.
38. Berberian G, Helguera G & Beauge L (1993) ATP activation of plasma membrane yeast H(+)-ATPase shows complex kinetics independently of the degree of purification. Biochim Biophys Acta 1153, 283-288.
39. Monteiro GA & Sa-Correia I (1998) In vivo activation of yeast plasma membrane H+-ATPase by ethanol: effect on the kinetic parameters and involvement of the carboxyl-terminus regulatory domain. Biochim Biophys Acta 1370, 310-316.
40. Eraso P, Mazon MJ & Portillo F (2006) Yeast protein kinase Ptk2 localizes at the plasma membrane and phosphorylates in vitro the C-terminal peptide of the H+-ATPase. Biochim Biophys Acta 1758, 164-170.
41. Gancedo C & Serrano R (1989) Energy yielding metabolism in yeast. In The Yeasts (Harrison JS & Rose AH, eds), pp. 205-259. Academic Press, New York.
42. Halasz A & Lasztity R (1991) Use of Yeast Biomass in Food Production. CRC Press, Boca Raton, FL.
43. Van der Rest ME, Kamminga AH, Nakano A, Anraku Y, Poolman B & Konings WN (1995) The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis. Microbiol Rev 59, 304-322.
44. Davidson JF & Schiestl RH (2001) Mitochondrial respiratory electron carriers are involved in oxidative stress during heat stress in Saccharomyces cerevisiae. Mol Cell Biol 21, 8483-8489.
45. Davidson JF, Whyte B, Bissinger PH & Schiestl RH (1996) Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93, 5116-5121.
46. Ueom J, Kwon S, Kim S, Chae Y & Lee K (2003) Acquisition of heat shock tolerance by regulation of intracellular redox states. Biochim Biophys Acta 1642, 9-16.
47. Postmus J, Canelas AB, Bouwman J, Bakker BM, van Gulik W, de Mattos MJ, Brul S & Smits GJ (2008) Quantitative analysis of the high temperature-induced glycolytic flux increase in Saccharomyces cerevisiae reveals dominant metabolic regulation. J Biol Chem 283, 23524-23532.
48. Tai SL, Daran-Lapujade P, Luttik MA, Walsh MC, Diderich JA, Krijger GC, van Gulik WM, Pronk JT & Daran JM (2007) Control of the glycolytic flux in Saccharomyces cerevisiae grown at low temperature: a multi-level analysis in anaerobic chemostat cultures. J Biol Chem 282, 10243-10251.
49. Chaplin MF & Bucke C (1990) Enzyme Technology. Cambridge University Press, Cambridge.
50. Stouthamer AH (1979) The search for correlation between theoretical and experimental growth yields. In International Review of Biochemistry and Microbial Biochemistry (Quayle JR, ed), pp. 1-47. University Park Press, Baltimore, MD.
51. Mensonides FIC, Bakker BM, Brul S, Hellingwerf KJ & Teixeira de Mattos MJ (2007) A kinetic model as a tool to understand the response of Saccharomyces cerevisiae to heat exposure. In Modelling Microorganisms in Food (Brul S, Van Gerwen S & Zwietering M, eds), pp. 228-249. Woodhead, Cambridge, UK.
52. 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.
53. Parrou JL & Francois J (1997) A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal Biochem 248, 186-188.
54. Postmus J (2011) The physiological response of Saccharomyces cerevisiae to temperature stress. PhD thesis, University of Amsterdam.
55. De Deken RH (1966) The Crabtree effect: a regulatory system in yeast. J Gen Microbiol 44, 149-156.
56. Pirt SJ (1965) The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci 163, 224-231.
57. Neijssel OM & Tempest DW (1976) Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture. Arch Microbiol 107, 215-221.
58. Pirt SJ (1982) Maintenance energy: a general model for energy-limited and energy-sufficient growth. Arch Microbiol 133, 300-302.
59. Hottiger T, Schmutz P & Wiemken A (1987) Heatinduced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169, 5518-5522.
60. Parrou JL, Teste MA & Francois J (1997) Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology 143, 1891-1900.