Abstract
Synthesis, storage, and degradation of nonpolar lipids enable cells to continue cell metabolism when nutrients are no longer provided by the environment. Major nonpolar lipids occurring in yeast are triacylglycerols and steryl esters. These hydrophobic molecules are sequestered from the cytosolic environment in the core of special organelles termed lipid droplets (lipid particles). When nutrients are no longer provided by the environment, hydrolytic enzymes catalyze the degradation of triacylglycerols and steryl esters. The respective breakdown products serve as energy source and/or building blocks for membrane formation. Here, enzymes catalyzing nonpolar lipid synthesis and degradation in the budding yeast Saccharomyces cerevisiae are described with special emphasis to their localization and regulation. Furthermore, examples are presented showing that the formation of lipid droplets is not only disturbed in cells defective in polypeptides directly involved in nonpolar lipid synthesis and degradation, but also in a number of mutants defective in polypeptides and pathways which are not obviously linked to nonpolar lipid turnover. Although research over the past decade provided major insights into nonpolar lipid metabolism, many aspects of nonpolar lipid synthesis, storage, and degradation remain to be elucidated. Research needs for a better understanding of nonpolar lipid turnover are outlined at the end of this chapter.
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References
Athenstaedt K, Daum G (2003) YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J Biol Chem 278:23317–23323
Athenstaedt K, Daum G (2005) Tgl4p and Tgl5p, two triacylglycerol lipases of the yeast Saccharomyces cerevisiae are localized to lipid particles. J Biol Chem 280:37301–37309
Athenstaedt K, Daum G (2006) The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci 63:1355–1369
Athenstaedt K, Daum G (2011) Lipid storage: yeast we can! Eur J Lipid Sci Technol 113:1188–1197
Choudhary V, Jacquier N, Schneiter R (2011) The topology of the triacylglycerol synthesizing enzyme Lro1 indicates that neutral lipids can be produced within the luminal compartment of the endoplasmatic reticulum: implications for the biogenesis of lipid droplets. Commun Integr Biol 4:781–784
Choudhary V, Ojha N, Golden A, Prinz WA (2015) A conserved family of proteins facilitates nascent lipid droplet budding from the ER. J Cell Biol 211:261–271
Connerth M, Czabany T, Wagner A, Zellnig G, Leitner E, Steyrer E, Daum G (2010) Oleate inhibits steryl ester synthesis and causes liposensitivity in yeast. J Biol Chem 285:26832–26841
Czabany T, Wagner A, Zweytick D, Lohner K, Leitner E, Ingolic E, Daum G (2008) Structural and biochemical properties of lipid particles from the yeast Saccharomyces cerevisiae. J Biol Chem 283:17065–17074
Dahlqvist A, Ståhl U, Lenman M, Banaś A, Lee M, Sandager L, Ronne H, Stymne S (2000) Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci U S A 97:6487–6492
Fei W, Alfaro G, Muthusamy B-P, Klaasen Z, Graham TR, Yang H, Beh CT (2008) Genome-wide analysis of sterol-lipid storage and trafficking in Saccharomyces cerevisiae. Eukaryot Cell 7:401–414
Gaspar ML, Jesch SA, Viswanatha R, Antosh AL, Brown WJ, Kohlwein SD, Henry SA (2008) A block in ER-to-Golgi trafficking inhibits phospholipid synthesis and induces neutral lipid accumulation. J Biol Chem 283:25735–25751
Ghosal A, Banaś A, Ståhl U, Dahlqvist A, Lindqvist Y, Stymne S (2007) Saccharomyces cerevisiae phospholipid:diacylglycerol acyl transferase (PDAT) devoid of its membrane anchor region is a soluble and active enzyme retaining its substrate specificities. Biochim Biophys Acta 1771:1457–1463
Ham HJ, Rho HJ, Shin SK, Yoon HJ (2010) The TGL2 gene of Saccharomyces cerevisiae encodes an active acylglycerol lipase located in the mitochondria. J Biol Chem 285:3005–3013
Heier C, Taschler U, Rengachari S, Oberer M, Wolinski H, Natter K, Kohlwein SD, Leber R, Zimmermann R (2010) Identification of Yju3p as functional orthologue of mammalian monoglyceride lipase in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1801:1063–1071
Horvath SE, Wagner A, Steyrer E, Daum G (2011) Metabolic link between phosphatidylethanolamine and triacylglycerol metabolism in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1811:1030–1037
Jandrositz A, Petschnigg J, Zimmermann R, Natter K, Scholze H, Hermetter A, Kohlwein SD, Leber R (2005) The lipid droplet enzyme Tgl1p hydrolyzes both steryl esters and triglycerides in the yeast, Saccharomyces cerevisiae. Biochim Biophys Acta 1735:50–58
Jensen-Pergakes K, Guo Z, Giattina M, Sturley SL, Bard M (2001) Transcriptional regulation of the two sterol esterification genes in the yeast Saccharomyces cerevisiae. J Bacteriol 183:4950–4957
Kamisaka Y, Tomita N, Kimura K, Kainou K, Uemura H (2007) DGA1 (diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the Δsnf2 disruptant of Saccharomyces cerevisiae. Biochem J 408:61–68
Klein I, Klug L, Schmidt C, Zandl M, Korber M, Daum G, Athenstaedt K (2016) Regulation of the yeast triacylglycerol lipases Tgl4p and Tgl5p by the presence/absence of nonpolar lipids. Mol Biol Cell 27:2014–2024
Koch B, Schmidt C, Daum G (2014a) Storage lipids of yeast: a survey of nonpolar lipid metabolism in Saccharomyces cerevisiae, Pichia pastoris, and Yarrowia lipolytica. FEMS Microbiol Rev 38:892–915
Koch B, Schmidt C, Ploier B, Daum G (2014b) Modifications of the C terminus affect functionality and stability of yeast triacylglycerol lipase Tgl3p. J Biol Chem 289:19306–19316
Kodaki T, Hosaka K, Nikiwa J, Yamashita S (1995) The SNF2/SWI2/GAM1/TYE3/RIC1 gene is involved in the coordinate regulation of phospholipid synthesis in Saccharomyces cerevisiae. J Biochem (Tokyo) 117:362–368
Köffel R, Schneiter R (2006) Yeh1 constitutes the major steryl ester hydrolase under heme-deficient conditions in Saccharomyces cerevisiae. Eukaryot Cell 5:1018–1025
Köffel R, Tiwari R, Falquet L, Schneiter R (2005) The Saccharomyces cerevisiae YLL012/YEH1, YLR020/YEH2, and TGL1 genes encode a novel family of membrane-anchored lipases that are required for steryl ester hydrolysis. Mol Cell Biol 25:1655–1668
Kurat CF, Natter K, Petschnigg J, Wolinski H, Scheuringer K, Scholz H, Zimmermann R, Leber R, Zechner R, Kohlwein SD (2006) Obese yeast: triglyceride lipolysis is functionally conserved from mammals to yeast. J Biol Chem 281:491–500
Kurat CF, Wolinski H, Petschnigg J, Kaluarachchi S, Andrews B, Natter K, Kohlwein SD (2009) Cdk1/Cdc28-dependent activation of the major triacylglycerol lipase Tgl4 in yeast links lipolysis to cell-cycle progression. Mol Cell 33:53–63
Müllner H, Deutsch G, Leitner E, Ingolic E, Daum G (2005) YEH2/YLR020c encodes a novel steryl ester hydrolase of the yeast Saccharomyces cerevisiae. J Biol Chem 280:13321–13328
O’Hara L, Han GS, Peak-Chew S, Grimsey N, Carman GM, Siniossoglou S (2006) Control of phospholipid synthesis by phosphorylation of the yeast lipin Pah1p/Smp2p Mg2+-dependent phosphatidate phosphatase. J Biol Chem 281:34537–34548
Oelkers P, Tinkelenberg A, Erdeniz N, Cromley D, Billheimer J, Sturley SL (2000) A lecithin cholesterol acyltransferase-like gene mediates diacylglycerol esterification in yeast. J Biol Chem 275:15609–15612
Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277:8877–8881
Ploier B, Scharwey M, Koch B, Schmidt C, Schatte J, Rechberger G, Kollroser M, Hermetter A, Daum G (2014) Screening for hydrolytic enzymes reveals Ayr1p as a novel triacylglycerol lipase in Saccharomyces cerevisiae. J Biol Chem 288:36061–36072
Rajakumari S, Daum G (2010a) Multiple functions as lipase, steryl ester hydrolase, phospholipase, and acyltransferase of Tgl4p from the yeast Saccharomyces cerevisiae. J Biol Chem 285:15769–15776
Rajakumari S, Daum G (2010b) Janus-faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21:501–510
Sandager L, Gustavsson MH, Ståhl U, Dahlqvist A, Wiberg E, Banaś A, Lenman M, Ronne H, Stymne S (2002) Storage lipid synthesis is non-essential in yeast. J Biol Chem 277:6478–6482
Schmidt C, Athenstaedt K, Koch B, Ploier B, Daum G (2013) Regulation of the yeast triacylglycerol lipase Tgl3p by formation of nonpolar lipids. J Biol Chem 288:19939–19948
Selvaraju K, Gowsalya R, Vijayakumar R, Nachiappan V (2016) MGL2/YMR210w encodes a monoacylglycerol lipase in Saccharomyces cerevisiae. FEBS Lett 590:1174–1186
Sorger D, Daum G (2002) Synthesis of triacylglycerols by the acyl-coenzyme A:diacyl-glycerol acyltransferase Dga1p in lipid particles of the yeast Saccharomyces cerevisiae. J Biol Chem 184:519–524
Ståhl U, Carlsson AS, Lenman M, Dahlqvist A, Wiberg E, Banaś W, Banaś A, Stymne S (2004) Cloning and characterization of a phospholipid:diacylglycerol acyltransferase from Arabidopsis. Plant Physiol 135:1324–1335
Szymanski KM, Binns D, Bartz R, Grishin NV, Li WP, Agarwal AK, Garg A, Anderson RG, Goodman JM (2007) The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc Natl Acad Sci U S A 104:20890–20895
Tiwari R, Köffel R, Schneiter R (2007) An acetylation/deacetylation cycle controls the export of sterols and steroids from S. cerevisiae. EMBO J 26:5109–5119
Wang CW (2015) Lipid droplet dynamics in budding yeast. Cell Mol Life Sci 72:2677–2695
Wang CW, Miao YH, Chang YS (2014) Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16. J Cell Sci 127:1214–1228
Wolinski H, Hofbauer HF, Hellauer K, Cristobal-Sarramian A, Kolb D, Radulovic M, Knittelfelder OL, Rechberger GN, Kohlwein SD (2015) Seipin is involved in the regulation of phosphatidic acid metabolism at a subdomain of the nuclear envelope in yeast. Biochim Biophys Acta 1851:1450–1464
Yang H, Bard M, Bruner DA, Gleeson A, Deckelbaum RJ, Aljinovic G, Pohl TM, Rothstein R, Sturley SL (1996) Sterol esterification in yeast: a two-gene process. Science 272:1353–1356
Yu C, Kennedy NJ, Chang CCY, Rothblatt J (1996) Molecular cloning and characterization of two isoforms of Saccharomyces cerevisiae acyl-CoA:sterol acyltransferases. J Biol Chem 271:24157–24163
Zweytick D, Leitner E, Kohlwein SD, Yu C, Rothblatt J, Daum G (2000) Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae. Eur J Biochem 267:1075–1082
Acknowledgment
This work was financially supported by the Austrian Science Fund (FWF) project P26308 to K.A.
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Athenstaedt, K. (2019). Players in the Nonpolar Lipid Game: Proteins Involved in Nonpolar Lipid Metabolism in Yeast. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50430-8_31
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