Cold response in Saccharomyces cerevisiae: New functions for old mechanisms

FEMS Microbiology Reviews

Volumn 31, Issue 3, 2007, Pages 327-341

  Aguilera, Jaime ^a   Randez Gil, Francisca ^a   Prieto, Jose Antonio ^a  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

Cold shock; Freezing; Signal transduction pathways; Signalling; Stress; Yeast

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL PROTEIN; GLYCEROL; HEAT SHOCK PROTEIN; PROTEIN KINASE C; PROTEIN OLE1; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MOX1; TRANSCRIPTION FACTOR MOX2; TRANSCRIPTION FACTOR MOX4; TREHALOSE; UNCLASSIFIED DRUG;

CARBOHYDRATE METABOLISM; COLD ACCLIMATIZATION; COLD SENSITIVITY; ENVIRONMENTAL TEMPERATURE; FREEZING; FUNGUS MUTANT; GENE EXPRESSION REGULATION; LOW TEMPERATURE; MEMBRANE FLUIDITY; NONHUMAN; PHYSIOLOGY; PROMOTER REGION; REVIEW; RIBOSOME; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRESS; TEMPERATURE DEPENDENCE; TIME; TRANSCRIPTOMICS;

COLD; FREEZING; HEAT-SHOCK PROTEINS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 34047124273     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2007.00066.x     Document Type: Review

References (144)

1. Abe F & Horikoshi K (2000) Tryptophan permease gene TAT2 confers high-pressure growth in Saccharomyces cerevisiae. Mol Cell Biol 20: 8093-8102.
2. Abramova N, Cohen BD, Sertil O, Kapoor R, Davis KJA & Lowry CV (2001a) Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodelling of the cell wall in Saccharomyces cerevisiae. Genetics 157: 1169-1177.
3. Abramova N, Sertil O, Mehta S & Lowry CV (2001b) Reciprocal regulation of anerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J Bacteriol 183: 2881-2887.
4. Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC & de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20: 1681-1691.
5. Aguilera J, Rodríguez-Vargas S & Prieto JA (2005) The HOG MAP kinase pathway is required for the induction of methylglyoxal-responsive genes and determines methylglyoxal resistance in Saccharomyces cerevisiae. Mol Microbiol 56: 228-239.
6. 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.
7. Ariño J, Pérez-Callejón E, Cunillera N, Camps M, Posas F & Ferrer A (1993) Protein phosphatases in higher plants: multiplicity of type 2A phosphatases in Arabidopsis thaliana. Plant Mol Biol 21: 475-485.
8. Auld KL, Brown CR, Casolari JM, Komili S & Silver PA (2006) Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates. Mol Cell 21: 861-871.
9. Beeser AE & Cooper TG (1999) The dual-specificity protein phosphatase Yvh1p acts upstream of the protein kinase Mck1p in promoting spore development in Saccharomyces cerevisiae. J Bacteriol 181: 5219-5224.
10. Beeser AE & Cooper TG (2000) The dual-specificity protein phosphatase Yvh1p regulates sporulation, growth, and glycogen accumulation independently of catalytic activity in Saccharomyces cerevisiae via the cyclic AMP-dependent protein kinase cascade. J Bacteriol 182: 3517-3528.
11. Blomberg A (2000) Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiol Lett 182: 1-8.
12. Bultynck G, Heath VL, Majeed AP, Galan JM, Haguenauer-Tsapis R & Cyert MS (2006) Slm1 and slm2 are novel substrates of the calcineurin phosphatase required for heat stress-induced endocytosis of the yeast uracil permease. Mol Cell Biol 26: 4729-4745.
13. Carratú L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L & Maresca B (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93: 3870-3875.
14. Chen X, Sullivan DS & Huffaker TC (1994) Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc Natl Acad Sci USA 91: 9111-9115.
15. Choi J-Y, Stukey J, Hwangs S-Y & Martin CE (1996) Regulatory elements that control transcription activation and unsaturated fatty acid-mediated repression of the Saccharomyces cerevisiae OLE1 gene. J Biol Chem 271: 3581-3589.
16. Chung N, Mao C, Heitman J, Hannun YA & Obeid LM (2001) Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J Biol Chem 276: 35614-35621.
17. Cohen BD, Sertil O, Abramova NE, Davies KJ & Lowry CV (2001) Induction and repression of DAN1 and the family of anaerobic mannoprotein genes in Saccharomyces cerevisiae occurs through a complex array of regulatory sites. Nucleic Acids Res 29: 799-808.
18. Craig EA & Jacobsen K (1985) Mutations in cognate genes of Saccharomyces cerevisiae hsp70 result in reduced growth rates at low temperatures. Mol Cell Biol 5: 3517-3524.
19. Davenport KR, Sohaskey M, Kamada Y, Levin DE & Gustin MC (1995) A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161.
20. de Jesus Ferreira MC, Bao X, Laizé V & Hohmann S (2001) Transposon mutagenesis reveals novel loci affecting tolerance to salt stress and growth at low temperature. Curr Genet 40: 27-39.
21. de Nadal E, Alepuz PM & Posas F (2002) Dealing with osmostress through MAP kinase activation. EMBO Rep 3: 735-740.
22. di Como CJ & Arndt KT (1996) Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev 10: 1904-1916.
23. Du X & Takagi H (2005) N-Acetyltransferase Mpr1 confers freeze tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. J Biochem 138: 391-397.
24. Düvel K, Santhanam A, Garrett S, Schneper L & Broach JR (2003) Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast. Mol Cell 11: 1467-1478.
25. Elbein AD, Pan YT, Pastuszak I & Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17R-27R.
26. Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24: 469-486.
27. Fauman EB & Saper MA (1996) Structure and function of protein tyrosine phosphatases. Trends Biochem Sci 21: 413-417.
28. Gancedo C & Flores CL (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4: 351-359.
29. García-Rodriguez LJ, Durán A & Roncero C (2000) Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions. J Bacteriol 182: 2428-2437.
30. Gast K, Damaschun G, Damaschun H, Misselwitz R & Zirwer D (1993) Cold denaturation of yeast phosphoglycerate kinase: kinetics of changes in secondary structure and compactness on unfolding and refolding. Biochemistry 32: 7747-7752.
31. Geissler S, Siegers K & Schiebel E (1998) A novel protein complex promoting formation of functional α- and γ-tubulin. EMBO J 17: 952-966.
32. Gon Y, Hashimoto S, Matsumoto K, Nakayama T, Takeshita I & Horie T (1998) Cooling and rewarming-induced IL-8 expression in human bronchial epithelial cells through p38 MAP kinase-dependent pathway. Biochem Biophys Res Commun 249: 156-160.
33. Greenway SC & Storey KB (2000) Activation of mitogen-activated protein kinases during natural freezing and thawing in the wood frog. Mol Cell Biochem 209: 29-37.
34. Griffioen G & Thevelein JM (2002) Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet 41: 199-207.
35. Griffioen G, Swinnen S & Thevelein JM (2003) Feedback inhibition on cell wall integrity signaling by Zds1 involves Gsk3 phosphorylation of a cAMP-dependent protein kinase regulatory subunit. J Biol Chem 278: 23460-23471.
36. Gualerzi CO, Giuliodori AM & Pon CL (2003) Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331: 527-539.
37. Gustin MC, Albertyn J, Alexander M & Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264-1300.
38. Hampsey M (1997) A review of phenotypes in Saccharomyces cerevisiae. Yeast 13: 1099-1133.
39. Harris DM, Myrick TL & Rundle SJ (1999) The Arabidopsis homolog of yeast TAP42 and mammalian α4 binds to the catalytic subunit of protein phosphatase 2A and is induced by chilling. Plant Physiol 121: 609-617.
40. Hayashi M & Maeda T (2006) Activation of the HOG pathway upon cold stress in Saccharomyces cerevisiae. J Biochem (Tokyo) 139: 797-803.
41. Healy AM, Zolnierowick S, Stapleton AE, Goebl M, DePaoli-Roach AA & Pringle JR (1991) CDC55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization, and homology to the β subunit of mammalian type 2A protein phosphatase. Mol Cell Biol 11: 5767-5780.
42. Heinisch JJ, Lorberg A, Schmitz HP & Jacoby JJ (1999) The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol Microbiol 32: 671-680.
43. Helliwell SB, Howald I, Barbet N & Hall MN (1998) TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics 148: 99-112.
44. Hirata Y, Andoh T, Asahara T & Kikuchi A (2003) Yeast glycogen synthase kinase-3 activates Msn2p-dependent transcription of stress responsive genes. Mol Biol Cell 14: 302-312.
45. Hohmann S (2002) Osmotic stress signalling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
46. Homma T, Iwahashi H & Komatsu Y (2003) Yeast gene expression during growth at low temperature. Cryobiology 46: 230-237.
47. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD & Jentsch S (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102: 577-586.
48. Hoppe T, Rape M & Jentsch S (2001) Membrane-bound transcription factors: regulated release by RIP or RUP. Curr Opin Cell Biol 13: 344-348.
49. Imai J, Toh-e A & Matsui Y (1996) Genetic analysis of the Saccharomyces cerevisiae RHO3 gene, encoding a Rho-type small GTPase, provides evidence for a role in bud formation. Genetics 142: 359-369.
50. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H & Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278: 12191-12198.
51. Inouye M (1999) Cold-shock response and adaptation. J Mol Microbiol Biotechnol 1: 191.
52. Jiang Y & Broach JR (1999) Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J 18: 2782-2792.
53. Jiang Y, Vasconcelles MJ, Wretzel S, Light A, Martin CE & Goldberg MA (2001) MGA2 is involved in the low-oxygen response element-dependent hypoxic induction of genes in Saccharomyces cerevisiae. Mol Cell Biol 21: 6161-6169.
54. Jiang Y, Vasconcelles MJ, Wretzel S, Light A, Gilooly L, McDaid K, Oh C-S, Martin CE & Goldberg MA (2002) Mga2p processing by hypoxia and unsaturated fatty acids in Saccharomyces cerevisiae: impact on LORE-dependent gene expression. Eukaryot Cell 1: 481-490.
55. Jones PG & Inouye M (1996) RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol Microbiol 21: 1207-1218.
56. Kajiwara S, Aritomi T, Suga K, Ohtaguchi K & Kobayashi O (2000) Overexpression of the OLE1 gene enhances ethanol fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53: 568-574.
57. Kamada Y, Jung US, Piotrowski J & 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.
58. Kandror O, Bretschneider N, Kreydin E, Cavalieri D & Goldberg AL (2004) Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13: 771-781.
59. Kim J, Alizadeh P, Harding T, Hefner-Gravink A & Klionsky DJ (1996) Disruption of the yeast ATH1 gene confers better survival after dehydration, freezing and ethanol shock: potential commercial applications. Appl Environ Microbiol 62: 1563-1569.
60. Laroche C, Beney L, Marechal PA & Gervais P (2001) The effect of osmotic pressure on the membrane fluidity of Saccharomyces cerevisiae at different physiological temperatures. Appl Microbiol Biotechnol 56: 249-254.
61. Lawrence CL, Botting CH, Antrobus R & Coote PJ (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24: 3307-3323.
62. Lee SJ & Baserga SJ (1997) Functional separation of pre-rRNA processing steps revealed by truncation of the U3 small nucleolar ribonucleoprotein component, Mpp10. Proc Natl Acad Sci USA 94: 13536-13541.
63. Lehman K, Rossi G, Adamo JE & Brennwald P (1999) Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J Cell Biol 146: 125-140.
64. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262-291.
65. Loertscher J, Larson LL, Matson CK, Parrish ML, Felthauser A, Sturm A, Tachibana C, Bard M & Wright R (2006) Endoplasmic reticulum-associated degradation is required for cold adaptation and regulation of sterol biosynthesis in the yeast Saccharomyces cerevisiae. Eukaryot Cell 5: 712-722.
66. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, Bonenfant D, Oppliger W, Jenoe P & Hall MN (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10: 457-468.
67. López CS, Heras H, Garda H, Ruzal S, Sánchez-Rivas C & Rivas E (2000) Biochemical and biophysical studies of Bacillus subtilis envelopes under hyperosmotic stress. Int J Food Microbiol 55: 137-142.
68. Los DA & Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142-157.
69. Manning BD, Padhmanabha R & Snyder M (1997) The Rho-GFP Rom2p localizes to sites of polarized cell grow and participates in cytoskeletal functions in Saccharomyces cerevisiae. Mol Biol Cell 8: 1829-1844.
70. Mansilla MC & de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol 183: 229-235.
71. Martínez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H & Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227-2235.
72. McKemy DD, Neuhausser WM & Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58.
73. Mikami K, Kanesaki Y, Suzuki I & Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46: 905-915.
74. Monroy AF, Sarhan F & Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression. Evidence for a role of calcium. Plant Physiol 102: 1227-1235.
75. Monroy AF, Sangwan V & Dhindsa RS (1998) Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. Plant J 13: 653-660.
76. Muda M, Manning ER, Orth K & Dixon JE (1999) Identification of the human YVH1 protein-tyrosine phosphatase orthologue reveals a novel zinc binding domain essential for in vivo function. J Biol Chem 274: 23991-23995.
77. Murata Y, Homma T, Kitagawa E et al. (2006) Genome-wide expression analysis of yeast response during exposure to 4°C. Extremophiles 10: 117-128.
78. Nakagawa Y, Sakumoto N, Kaneko Y & Harashima S (2002) Mga2p is a putative sensor for low temperature and oxygen to induce OLE1 transcription in Saccharomyces cerevisiae. Biochem Biophys Res Commun 291: 707-713.
79. Nakagawa Y, Ueda A, Kaneko Y & Harashima S (2003) Merging of multiple signals regulating Δ9 fatty acid desaturase gene transcription in Saccharomyces cerevisiae. Mol Gen Genomics 269: 370-380.
80. Noguchi E, Kayashi N, Nakashima N & Nishimoto T (1997) Yrb2p, a Nup2p-related yeast protein, has a functional overlap with Rna1p, a yeast Ran-GTPase-activating protein. Mol Cell Biol 17: 2235-2246.
81. Noguchi E, Sayito Y, Saber S & Nishimoto T (1999) Disruption of the YRB2 gene retards nuclear protein export, causing a profound mitotic delay, and can be rescued by overexpression of XPO1/CRM1. J Biochem 125: 574-585.
82. Odani M, Komatsu Y, Oka S & Iwahashi H (2003) Screening of genes that respond to cryopreservation stress using yeast DNA microarray. Cryobiology 47: 155-164.
83. Ohsaka Y, Ohgiya S, Hoshino T & Ishizaki K (2002) Phosphorylation of c-Jun N-terminal kinase in human hepatoblastoma cells is transiently increased by cold exposure and further enhanced by subsequent warm incubation of the cells. Cell Physiol Biochem 12: 111-118.
84. Örvar BL, Sangwan V, Omann F & Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23: 785-794.
85. Panadero J, Pallotti C, Rodríguez-Vargas S, Randez-Gil F & Prieto JA (2006) A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J Biol Chem 281: 4638-4645.
86. Papp E, Nardai G, Soti C & Csermely P (2003) Molecular chaperones, stress proteins and redox homeostasis. Biofactors 17: 249-257.
87. Park JI, Grant CM, Attfield PV & Dawes IW (1997) The freeze-thaw stress response of the yeast Saccharomyces cerevisiae is growth phase specific and is controlled by nutritional state via the RAS-cyclic AMP signal transduction pathway. Appl Environ Microbiol 63: 3818-3824.
88. Park JI, Collinson EJ, Grant CM & Dawes IW (2005a) Rom2p, the Rho1 GTP/GDP exchange factor of Saccharomyces cerevisiae, can mediate stress responses via the Ras-cAMP pathway. J Biol Chem 280: 2529-2535.
89. Park JI, Grant CM & Dawes IW (2005b) The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras-cyclic AMP pathway in stress responses. Biochem Biophys Res Commun 327: 311-319.
90. Parrou JL, Teste MA & François 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.
91. Peier AM, Moqrich A, Hergarden AC et al. (2002) ATRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
92. Platt A & Reece RJ (1998) The yeast galactose genetic switch is mediated by the formation of a Gal4p-Gal80p-Gal3p complex. EMBO J 17: 4086-4091.
93. Randez-Gil F, Aguilera J, Codón A, Rincón AM, Estruch F & Prieto JA (2003) Baker's yeast: challenges and future aspects. Functional Genetics of Industrial Yeasts (de Winde JH, ed), pp. 57-97. Springer-Verlag, Heidelberg.
94. Revardel E & Aigle M (1993) The NUM1 yeast gene: length polymorphism and physiological aspects of mutant phenotype. Yeast 9: 495-506.
95. Reynolds TB, Hopkins BD, Lyons MR & Graham TR (1998) The high osmolarity glycerol response (HOG) MAP kinase pathway controls localization of a yeast golgi glycosyltransferase. J Cell Biol 143: 935-946.
96. κB and MAP kinase cascades by hypothermic stress in endothelial cells. Cryobiology 44: 161-169.
97. Rodríguez-Vargas S, Sánchez-García A, Martínez-Rivas JM, Prieto JA & Randez-Gil F (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73: 110-116.
98. Rohde JR, Campbell S, Zurita-Martinez SA, Cutler NS, Ashe M & Cardenas ME (2004) TOR controls transcriptional and translational programs via Sap-Sit4 protein phosphatase signaling effectors. Mol Cell Biol 24: 8332-8341.
99. Sahara T, Goda T & Ohgiya S (2002) Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. J Biol Chem 277: 50015-50021.
100. Sakumoto N, Mukai Y, Uchida K et al. (1999) A series of protein phosphatase gene disruptants in Saccharomyces cerevisiae. Yeast 15: 1669-1679.
101. Sangwan V, Örvar BL, Beyerly J, Hirt H & Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31: 629-638.
102. Santangelo GM (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 253-282.
103. Santhanam A, Hartley A, Düvel K, Broach JR & Garrett S (2004) PP2A phosphatase activity is required for stress and Tor kinase regulation of yeast stress response factor Msn2p. Eukaryot Cell 3: 1261-1271.
104. Schade B, Jansen G, Whiteway M, Entian KD & Thomas DY (2004) Cold adaptation in budding yeast. Mol Biol Cell 15: 5492-5502.
105. Schmelzle T & Hall MN (2000) TOR, a central controller of cell growth. Cell 103: 253-262.
106. Schmelzle T, Beck T, Martin DE & Hall MN (2004) Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol Cell Biol 24: 338-351.
107. Schmidt A, Kunz J & Hall MN (1996) TOR2 is required for organization of the actin cytoskeleton in yeast. Proc Natl Acad Sci USA 93: 13780-13785.
108. Schmidt A, Beck T, Koller A, Kunz J & Hall MN (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J 17: 6924-6931.
109. Schwartz MA & Madhani HD (2004) Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu Rev Genet 38: 725-748.
110. Seki M, Ishida J, Narusaka M et al. (2002a) Abstract monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2: 282-291.
111. Seki M, Narusaka M, Ishida J et al. (2002b) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
112. Seki M, Satou M, Sakurai T et al. (2004) RIKEN Arabidopsis full-length (RAFL) cDNA and its applications for expression profiling under abiotic stress conditions. J Exp Bot 55: 213-223.
113. Shinozaki K & Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7: 161-167.
114. Siegers K, Waldmann T, Leroux MR, Grein K, Shevchenko A, Schiebel E & Hartl FU (1999) Compartmentation of protein folding in vivo: sequestration of non-native polypeptide by the chaperonin-GimC system. EMBO J 8: 75-84.
115. Singer MA & Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16: 460-468.
116. Skrzypek MS, Nagiec MM, Lester RL & Dickson RC (1998) Inhibition of amino acid transport by sphingoid long chain bases in Saccharomyces cerevisiae. J Biol Chem 273: 2829-2834.
117. Soto T, Beltrán FF, Paredes V, Madrid M, Millar JBA, Vicente-Soler J, Cansado J & Gacto M (2002) Cold induces stress-activated protein kinase-mediated response in the fission yeast Schizosaccharomyces pombe. Eur J Biochem 269: 5056-5065.
118. Stoldt V, Rademacher F, Kehren V, Ernst JF, Pearce DA & Sherman F (1996) Review: the Cct eukaryotic chaperonin subunits of Saccharomyces cerevisiae and other yeasts. Yeast 12: 523-529.
119. Stukey JE, McDonough VM & Martin CE (1989) Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J Biol Chem 264: 16537-16544.
120. Stukey JE, McDonough VM & Martin CE (1990) The OLE1 gene of Saccharomyces cerevisiae encodes the Δ9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. J Biol Chem 265: 20144-20149.
121. Suzuki I, Los DA, Kanesaki Y, Mikami K & Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19: 1327-1334.
122. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M & Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40: 235-244.
123. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL & Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15: 141-152.
124. Thevelein JM & de Winde JH (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33: 904-918.
125. Thieringer HA, Jones PG & Inouye M (1998) Cold shock and adaptation. BioEssays 20: 49-57.
126. Tokishita S & Mizuno T (1994) Transmembrane signal transduction by the Escherichia coli osmotic sensor, EnvZ: intermolecular complementation of transmembrane signalling. Mol Microbiol 13: 435-444.
127. van der Heide T & Poolman B (2000) Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc Natl Acad Sci USA 97: 7102-7106.
128. van der Heide T, Stuart MC & Poolman B (2001) On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine. EMBO J 20: 7022-7032.
129. van Dijck P, Ma P, Versele M, Gorwa M-F, Colombo S, Lemaire K, Bossi D, Loïez A & Thevelein JM (2000) A baker's yeast mutant (fil1) with a specific, partially inactivating mutation in adenylate cyclase maintains a high stress resistance during active fermentation and growth. J Mol Microbiol Biotechnol 2: 521-530.
130. Vasconcelles MJ, Jiang Y, McDaid K, Gilooly L, Wretzel S, Porter DL, Martin CE & Goldberg MA (2001) Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes. J Biol Chem 276: 14374-14384.
131. Vigh L, Maresca B & Harwood JL (1998) Does the membrane's physical state control the expression of heat shock and other genes? Trends Biochem Sci 23: 369-374.
132. Wang Y, Pierce M, Schneper L, Guldal CG, Zhang X, Tavazoie S & Broach JR (2004) Ras and Gpa2 mediate one branch of a redundant glucose signaling pathway in yeast. PLoS Biol 2: 610-622.
133. Westfall PJ, Ballon DR & Thorner J (2004) When the stress of your environment makes you go HOG wild. Science 306: 1511-1512.
134. Wilson WA & Roach PJ (2002) Nutrient-regulated protein kinases in budding yeast. Cell 111: 155-158.
135. Winkler A, Arkind C, Mattison CP, Burkholder A, Knoche K & Ota I (2002) Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress. Eukaryot Cell 1: 163-173.
136. Winzeler EA, Shoemaker DD, Astromoff A et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
137. Wolfe J & Bryant G (1999) Freezing, crying, and/or vitrification of membrane-solute-water systems. Cryobiology 39: 103-129.
138. Wullschleger S, Loewith R & Hall MN (2006) TOR signalling in growth and metabolism. Cell 124: 471-484.
139. Young JC, Barral JM & Hartl FU (2003) More than folding: localized functions of cytosolic chaperones. Trends Biochem Sci 28: 541-547.
140. Zenke FT, Engles R, Vollenbroich V, Meyer J, Hollenberg CP & Breunig KD (1996) Activation of Gal4p by galactose-dependent interaction of galactokinase and Gal80p. Science 272: 1662-1665.
141. Zhang L, Ohta A, Horiuchi H, Takagi M & Imai R (2001) Multiple mechanisms regulate expression of low temperature responsive (LOT) genes in Saccharomyces cerevisiae. Biochem Biophys Res Commun 283: 531-535.
142. Zhang L, Onda K, Imai R, Fukuda R, Horiuchi H & Ohta A (2003) Growth temperature downshift induces antioxidant response in Saccharomyces cerevisiae. Biochem Biophys Res Commun 307: 308-314.
143. Zhang S, Skalsky Y & Garfinkel DJ (1999) MGA2 or SPT23 is required for transcription of the 9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 151: 473-483.
144. Zhu H, Bilgin M, Bangham R et al. (2001) Global analysis of protein activities using proteome chips. Science 293: 2101-2105.