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Role of Sterol Metabolism and Endoplasmic Reticulum-Associated Degradation of Proteins in Cold Adaptation of Yeasts

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Cold-adapted Yeasts

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Abstract

The environmental conditions of organisms have significant impact on their ability to grow and thrive. This chapter summarizes recent research related to the understanding of cellular mechanisms necessary for psychrophilic yeasts to overcome molecular challenges present in low-temperature environments. In an effort to identify adaptive mechanisms that allow psychrophilic yeasts to thrive in cold environments, a high number of studies have been done to investigate the low-temperature response of Saccharomyces cerevisiae. The focus of this chapter is on evidence that the endoplasmic reticulum-associated degradation (ERAD) pathway and membrane metabolism regulation are connected to the cellular response and adaptation to low temperature in yeasts. Specific consideration is given to three genes in the ERAD pathway, UBC7, CUE1, and DOA10, which play a role in cold adaptation and regulating membrane composition in S. cerevisiae.

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References

  • Anderson RG, Orci L, Brown MS, Garcia-Segura LM, Goldstein JL (1983) Ultrastructural analysis of crystalloid endoplasmic reticulum in UT-1 cells and its disappearance in response to cholesterol. J Cell Sci 63:1–20

    PubMed  CAS  Google Scholar 

  • Atomi H, Sato T, Kanai T (2011) Application of hyperthermophiles and their enzymes. Curr Opin Biotechnol 22:618–626

    Article  PubMed  CAS  Google Scholar 

  • Basson ME, Thorsness M, Rine J (1986) Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc Natl Acad Sci USA 83:5563–5567

    Article  PubMed  CAS  Google Scholar 

  • Bays NW, Gardner RG, Seelig LP, Joazeiro CA, Hampton RY (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat Cell Biol 3:24–29

    Article  PubMed  CAS  Google Scholar 

  • Braun S, Matuschewski K, Rape M, Thoms S, Jentsch S (2002) Role of the ubiquitin-selective CDC48 (UFD1/NPL4) chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J 21:615–621

    Article  PubMed  CAS  Google Scholar 

  • Brock TD (1997) The value of basic research: discovery of Thermus aquaticus and other extreme thermophiles. Genetics 146:1207–1210

    PubMed  CAS  Google Scholar 

  • Brodsky JL, McCracken AA (1999) ER protein quality control and proteasome-mediated protein degradation. Semin Cell Dev Biol 10:507–513

    Article  PubMed  CAS  Google Scholar 

  • Brown MS, Goldstein JL (1980) Multivalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth. J Lipid Res 21:505–517

    PubMed  CAS  Google Scholar 

  • Burg JS, Espenshade PJ (2011) Regulation of HMG-CoA reductase in mammals and yeast. Prog Lipid Res 50:403–410

    Article  PubMed  CAS  Google Scholar 

  • Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241

    Article  PubMed  CAS  Google Scholar 

  • Cavicchioli R, Thomas T, Curmi PM (2000) Cold stress response in Archaea. Extremophiles 4:321–331

    Article  PubMed  CAS  Google Scholar 

  • Claessen JH, Kundrat L, Ploegh HL (2012) Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 22:22–32

    Article  PubMed  CAS  Google Scholar 

  • Daum G, Lees ND, Bard M, Dickson R (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14:1471–1510

    Article  PubMed  CAS  Google Scholar 

  • Donald KA, Hampton RY, Fritz IB (1997) Effects of overproduction of the catalytic domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase on squalene synthesis in Saccharomyces cerevisiae. Appl Environ Microbiol 63:3341–3344

    PubMed  CAS  Google Scholar 

  • Egner R, Rosenthal FE, Kralli A, Sanglard D, Kuchler K (1998) Genetic separation of FK506 susceptibility and drug transport in the yeast Pdr5 ATP-binding cassette multidrug resistance transporter. Mol Biol Cell 9:523–543

    Article  PubMed  CAS  Google Scholar 

  • Finegold L (1986) Molecular aspects of adaptation to extreme cold environments. Adv Space Res 6:257–264

    Article  PubMed  CAS  Google Scholar 

  • Gardner RG, Hampton RY (1999) A highly conserved signal controls degradation of 3-hydroxy-3-methylglutaryl-coenzyme A (HMG-CoA) reductase in eukaryotes. J Biol Chem 274:31671–31678

    Article  PubMed  CAS  Google Scholar 

  • Gasch A, Werner-Washburne M (2002) The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics 2:181–192

    Article  PubMed  CAS  Google Scholar 

  • Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430

    Article  PubMed  CAS  Google Scholar 

  • Goldstein JL, DeBose-Boyd RA, Brown MS (2006) Protein sensors for membrane sterols. Cell 124:35–46

    Article  PubMed  CAS  Google Scholar 

  • Haas AL, Siepmann TJ (1997) Pathways of ubiquitin conjugation. FASEB J 11:1257–1268

    PubMed  CAS  Google Scholar 

  • Hampton RY (2002) ER-associated degradation in protein quality control and cellular regulation. Curr Opin Cell Biol 14:476–482

    Article  PubMed  CAS  Google Scholar 

  • Hampton RY, Rine J (1994) Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J Cell Biol 125:299–312

    Article  PubMed  CAS  Google Scholar 

  • Hampton R, Dimster-Denk D, Rine J (1996a) The biology of HMG-CoA reductase: the pros of contra-regulation. Trends Biochem Sci 21:140–145

    PubMed  CAS  Google Scholar 

  • Hampton RY, Gardner RG, Rine J (1996b) Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol Biol Cell 7:2029–2044

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1992) The ubiquitin system for protein degradation. Annu Rev Biochem 61:761–807

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Hiraishi H, Mochizuki M, Takagi H (2006) Enhancement of stress tolerance in Saccharomyces cerevisiae by overexpression of ubiquitin ligase Rsp5 and ubiquitin-conjugating enzymes. Biosci Biotechnol Biochem 70:2762–2765

    Article  PubMed  CAS  Google Scholar 

  • Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458:453–460

    Article  PubMed  CAS  Google Scholar 

  • Hitchcock AL, Auld K, Gygi SP, Silver PA (2003) A subset of membrane-associated proteins is ubiquitinated in response to mutations in the endoplasmic reticulum degradation machinery. Proc Natl Acad Sci USA 100:12735–12740

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ignea C, Trikka FA, Kourtzelis I, Argiriou A, Kanellis AK, Kampranis SC, Makris AM (2012) Positive genetic interactors of HMG2 identify a new set of genetic perturbations for improving sesquiterpene production in Saccharomyces cerevisiae. Microb Cell Fact 11:162

    Article  PubMed  CAS  Google Scholar 

  • Inniss WE (1975) Interaction of temperature and psychrophilic microorganisms. Annu Rev Microbiol 29:445–465

    Article  PubMed  CAS  Google Scholar 

  • Koning AJ, Roberts CJ, Wright RL (1996) Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations. Mol Biol Cell 7:769–789

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, Brown A, Ellison J, Ohno K, Rosenfeld MA, Tagle DA, Pentchev PG, Pavan WJ (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277:232–235

    Article  PubMed  CAS  Google Scholar 

  • Lorenz RT, Parks LW (1987) Regulation of ergosterol biosynthesis and sterol uptake in a sterol-auxotrophic yeast. J Bacteriol 169:3707–3711

    PubMed  CAS  Google Scholar 

  • Lum PY, Wright R (1995) Degradation of HMG-CoA reductase-induced membranes in the fission yeast, Schizosaccharomyces pombe. J Cell Biol 131:81–94

    Article  PubMed  CAS  Google Scholar 

  • Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361

    Article  PubMed  Google Scholar 

  • McCracken AA, Brodsky JL (2003) Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). BioEssays 25:868–877

    Article  PubMed  CAS  Google Scholar 

  • Metzger MB, Maurer MJ, Dancy BM, Michaelis S (2008) Degradation of a cytosolic protein requires endoplasmic reticulum-associated degradation machinery. J Biol Chem 283:32302–32316

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi M, Goldstein JL, Brown MS (1988) Multivalent control of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Mevalonate-derived product inhibits translation of mRNA and accelerates degradation of enzyme. J Biol Chem 263:8929–8937

    PubMed  CAS  Google Scholar 

  • Nicholson RC, Williams DB, Moran LA (1990) An essential member of the HSP70 gene family of Saccharomyces cerevisiae is homologous to immunoglobulin heavy chain binding protein. Proc Natl Acad Sci USA 87:1159–1163

    Article  PubMed  CAS  Google Scholar 

  • Normington K, Kohno K, Kozutsumi Y, Gething MJ, Sambrook J (1989) S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57:1223–1236

    Article  PubMed  CAS  Google Scholar 

  • Parrish ML, Sengstag C, Rine JD, Wright RL (1995) Identification of the sequences in HMG-CoA reductase required for karmellae assembly. Mol Biol Cell 6:1535–1547

    Article  PubMed  CAS  Google Scholar 

  • Passmore LA, Barford D (2004) Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem J 379:513–525

    Article  PubMed  CAS  Google Scholar 

  • Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695:55–72

    Article  PubMed  CAS  Google Scholar 

  • Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Ariño J (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275:17249–17255

    Article  PubMed  CAS  Google Scholar 

  • Rice C, Cooke M, Treloar N, Vollbrecht P, Stukey J, McDonough V (2010) A role for MGA2, but not SPT23, in activation of transcription of ERG1 in Saccharomyces cerevisiae. Biochem Biophys Res Commun 403:293–297

    Article  PubMed  CAS  Google Scholar 

  • Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266

    Article  PubMed  CAS  Google Scholar 

  • Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529

    Article  PubMed  CAS  Google Scholar 

  • Russell NJ (2008) Membrane components and cold sensing. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 177–190

    Chapter  Google Scholar 

  • Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192:289–318

    Article  PubMed  CAS  Google Scholar 

  • Simpson CE, Ashe MP (2012) Adaptation to stress in yeast: to translate or not? Biochem Soc Trans 40:794–799

    Article  PubMed  CAS  Google Scholar 

  • Siperstein MD, Fagan VM (1966) Feedback control of mevalonate synthesis by dietary cholesterol. Journal Biol Chem 241:602–609

    CAS  Google Scholar 

  • Stetter KO (2006) Hyperthermophiles in the history of life. Philos Trans R Soc Lond B Biol Sci 361:1837–1844

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Swan TM, Watson K (1998) Stress tolerance in a yeast sterol auxotroph: role of ergosterol, heat shock proteins and trehalose. FEMS Microbiol Lett 169:191–197

    Article  PubMed  CAS  Google Scholar 

  • Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258

    Article  PubMed  CAS  Google Scholar 

  • Vashist S, Ng DT (2004) Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J Cell Biol 165:41–52

    Article  PubMed  CAS  Google Scholar 

  • Veen M, Stahl U, Lang C (2003) Combined overexpression of genes of the ergosterol biosynthetic pathway leads to accumulation of sterols in Saccharomyces cerevisiae. FEMS Yeast Res 4:87–95

    Article  PubMed  CAS  Google Scholar 

  • Vembar SS, Brodsky JL (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9:944–957

    Article  PubMed  CAS  Google Scholar 

  • Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–1086

    Article  PubMed  CAS  Google Scholar 

  • Watson K, Arthur H (1976) Leucosporidium yeasts: obligate psychrophiles which alter membrane-lipid and cytochrome composition with temperature. J Gen Microbiol 97:11–18

    Article  PubMed  CAS  Google Scholar 

  • Welch WJ, Suhan JP (1985) Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol 101:1198–1211

    Article  PubMed  CAS  Google Scholar 

  • Willey JM, Sherwood LM, Prescott LM (2008) Prescott, Harley, and Klein’s Microbiology, 7th edn. McGraw-Hill Higher Education, New York

    Google Scholar 

  • Wolf DH, Fink GR (1975) Proteinase C (carboxypeptidase Y) mutant of yeast. J Bacteriol 123:1150–1156

    PubMed  CAS  Google Scholar 

  • Wright R (1993) Insights from inducible membranes. Curr Biol 3:870–873

    Article  PubMed  CAS  Google Scholar 

  • Wright R, Basson M, D’Ari L, Rine J (1988) Increased amounts of HMG-CoA reductase induce “karmellae”: a proliferation of stacked membrane pairs surrounding the yeast nucleus. J Cell Biol 107:101–114

    Article  PubMed  CAS  Google Scholar 

  • Wright R, Keller G, Gould SJ, Subramani S, Rine J (1990) Cell-type control of membrane biogenesis induced by HMG-CoA reductase. New Biol 2:915–921

    PubMed  CAS  Google Scholar 

  • Wright R, Parrish ML, Cadera E, Larson L, Matson CK, Garrett-Engele P, Armour C, Lum PY, Shoemaker DD (2003) Parallel analysis of tagged deletion mutants efficiently identifies genes involved in endoplasmic reticulum biogenesis. Yeast 20:881–892

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Skalsky Y, Garfinkel DJ (1999) MGA2 or SPT23 is required for transcription of the Δ9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 151:473–483

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, Cell Biology and Development, University of Minnesota, 420 Washington Ave. SE 3-104 MCB, Minneapolis, MN, 55455, USA

    Kelaine Haas

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  1. Kelaine Haas
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Correspondence to Kelaine Haas .

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Editors and Affiliations

  1. Department of Agricultural, Environmental and Food Sciences, University of Perugia, Industrial Yeasts Collection DBVPG, Perugia, Italy

    Pietro Buzzini

  2. University of Innsbruck, Institute of Microbiology, Innsbruck, Austria

    Rosa Margesin

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Haas, K. (2014). Role of Sterol Metabolism and Endoplasmic Reticulum-Associated Degradation of Proteins in Cold Adaptation of Yeasts. In: Buzzini, P., Margesin, R. (eds) Cold-adapted Yeasts. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39681-6_13

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