Abstract
Lipids are the best known form of energy storage. Apart from being energy reserves and signaling molecules, they also form an integral part of the cell membranes and provide structure and fluidity to the membranes. A group of polar lipids, namely, the phospholipids (PLs), are membrane constituents, defining the structure, shape, and function of the cells. They decide the cell permeability due to their hydrophobicity. PLs also play an under-rated role in many human diseases, due to which more importance needs to be given toward studies focusing on their synthesis, function, and metabolism. The budding yeast, Saccharomyces cerevisiae, is a model organism for the study of PLs as it is a simple system to characterize lipid metabolic changes under various physiological conditions. Yeasts have been used to study the mechanisms related to lipid metabolism, lipid trafficking, and localization in different subcellular organelles. It also shows the presence of various PLs, which makes it a versatile tool for research. With the recent developments in detection and quantification of PLs, and techniques using novel reagents, tags, and specific stains to localize a particular lipid in different subcellular compartments, yeast makes itself a remarkable model for lipid research. In this chapter, we discuss the various PLs present in the budding yeast, their traffic within the yeast cell, and methods of tracking them.
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References
Fahy E, Subramaniam S, Brown HA, Glass CK, Merrill AH Jr, Murphy RC, Raetz CR, Russell DW, Seyama Y, Shaw W, Shimizu T, Spener F, van Meer G, VanNieuwenhze MS, White SH, Witztum JL, Dennis EA (2005) A comprehensive classification system for lipids. J Lipid Res 46:839–861
Bittman R (2013) Glycerolipids: chemistry. In: Roberts GCK (ed) Encyclopedia of biophysics. Springer, Berlin
Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6(5):227–233
Taylor CL (2003) Phosphatidylserine and cognitive dysfunction and dementia (qualified health claim: final decision letter). Center for Food Safety and Applied Nutrition, USFDA. Retrieved 23 Aug 2014
Lands WE (1965) Lipid metabolism. Annu Rev Biochem 34:313–346
Wang B, Tontonoz P (2019) Phospholipid remodelling in physiology and disease. Annu Rev Physiol 81(1):165–188
Schneiter R, Kohlwein SD (1997) Organelle structure, function, and inheritance in yeast: a role for fatty acid synthesis? Cell 88:431–434
Raychaudhuri S, Young BP, Espenshade PJ, Loewen C Jr (2012) Regulation of lipid metabolism: a tale of two yeasts. Curr Opin Cell Biol Aug 24(4):502–508
Klug L, Daum G (2014) Yeast lipid metabolism at a glance. FEMS Yeast Res 14:369–388
Singh P (2016) Budding yeast: an ideal backdrop for in vivo lipid biochemistry. Front Cell Dev Biol 4:156. https://doi.org/10.3389/fcell.2016.00156
Claypool SM, Koehler CM (2012) The complexity of cardiolipin in health and disease. Trends Biochem Sci 37:32–41
Schuiki I, Daum G (2009) Phosphatidylserine decarboxylases, key enzymes of lipid metabolism. IUBMB Life 61:151–162
Lands WE (1960) Metabolism of glycerolipids. 2. The enzymatic acylation of lysolecithin. J Biol Chem 235:2233–2237
Wagner S, Paltauf F (1994) Generation of glycerophospholipid molecular species in the yeast Saccharomyces cerevisiae. Fatty acid pattern of phospholipid classes and selective acyl turnover at sn-1 and sn-2 positions. Yeast 10(11):1429–1437
Fido M, Wagner S, Mayr H, Kohlwein SD, Paltauf F (1996) NATO ASI series. In: Op den Kamp JAF (ed) Molecular dynamics of biomembranes, vol H 96. Springer, Heidelberg, pp 315–326
Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42
Yeagle PL (2016) Lipid protein interactions in membranes. In: Yeagle PL (ed) The membrane of cells, 3rd edn. Academic, New York
Chang S-C, Heacock PN, Clancey CJ, Dowhan W (1998a) The PEL1 gene (renamed PGS1) encodes the phosphatidylglycerophosphate synthase of Saccharomyces cerevisiae. J Biol Chem 273:9829–9836
Osman C, Haag M, Wieland FT, Brugger B, Langer T (2010) A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J 29:1976–1987
Chang S-C, Heacock PN, Mileykovskaya E, Voelker DR, Dowhan W (1998b) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J Biol Chem 273:14933–14941
Tuller G, Hrastnik C, Achleitner G, Schiefthaler U, Klein F, Daum G (1998) YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett 421:15–18
Pangborn MC (1947) The composition of cardiolipin. J Biol Chem 168:351–361
Lecocq J, Ballou CE (1964) On the structure of cardiolipin. Biochemistry 3:976–980
Dimmer KS, Scorrano L (2006) (De)constructing mitochondria: what for? Physiology (Bethesda, Md) 21:233–241
Joshi AS, Thompson MN, Fei N, Huttemann M, Greenberg ML (2012) Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae. J Biol Chem 287:17589–17597
Beyer K, Klingenberg M (1985) ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance. Biochemistry 24(15):3821–3826
Lange C, Nett JH, Trumpower BL, Hunte C (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J 20:6591–6600
Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, Klingenberg M, Pfanner N, Greenberg ML (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275:22387–22394
Gohil VM, Thompson MN, Greenberg ML (2005) Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine and cardiolipin biosynthetic pathways in Saccharomyces cerevisiae. J Biol Chem 280:35410–35416
Schlame M, Rustow B (1990) Lysocardiolipin formation and reacylation in isolated rat liver mitochondria. Biochem J 272:589–595
Xu Y, Kelley RI, Blanck TJ, Schlame M (2003) Remodeling of cardiolipin by phospholipid transacylation. J Biol Chem 278:51380–51385
Schlame M, Kelley RI, Feigenbaum A, Towbin JA, Heerdt PM, Schieble T, Wanders RJ, DiMauro S, Blanck TJ (2003) Phospholipid abnormalities in children with Barth syndrome. J Am Coll Cardiol 42:1994–1999
Vreken P, Valianpour F, Nijtmans LG, Grivell LA, Plecko B, Wanders RJ, Barth PG (2000) Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. BiochemBiophys Res Commun 279:378–382. https://doi.org/10.1006/bbrc.2000.3952
Beranek A, Rechberger G, Knauer H, Wolinski H, Kohlwein SD, Leber R (2009) Identification of a cardiolipin-specific phospholipase encoded by the gene CLD1 (YGR110W) in yeast. J Biol Chem 284(17):11572–11578
Rijken PJ, Houtkooper RH, Akbari H, Brouwers JF, Koorengevel MC, de Kruijff B, Frentzen M, Vaz FM, de Kroon AI (2009) Cardiolipin molecular species with shorter acyl chains accumulate in Saccharomyces cerevisiae mutants lacking the acyl coenzyme A-binding protein Acb1p: new insights into acyl chain remodeling of cardiolipin. J Biol Chem 284:27609–27619
Ye C, Lou W, Li Y, Chatzispyrou IA, Huttemann M, Lee I, Houtkooper RH, Vaz FM, Chen S, Greenberg ML (2014) Deletion of the cardiolipin-specific phospholipase Cld1 rescues growth and life span defects in the tafazzin mutant: implications for Barth syndrome. J Biol Chem 289:3114–3125
Pokorna L, Cermakova P, Horvath A, Baile MG, Claypool SM, Griac P, Malinsky J, Balazova M (2015) Specific degradation of phosphatidylglycerol is necessary for proper mitochondrial morphology and function. Biochim Biophys Acta 1857:34–45
Nie J, Hao X, Chen D, Han X, Chang Z, Shi Y (2010) A novel function of the human CLS1 in phosphatidylglycerol synthesis and remodeling. Biochim Biophys Acta 1801:438–445
Lee SJ, Zhang J, Choi AM, Kim HP (2013) Mitochondrial dysfunction induces formation of lipid droplets as a generalized response to stress. Oxidative Med Cell Longev 2013:327167
Zweytick D, Athenstaedt K, Daum G (2000) Intracellular lipid particles of eukaryotic cells. Biochim Biophys Acta 1469:101–120
Farese RV Jr, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139:855–860
Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438
Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J Biol Chem 277:44507–44512
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
Novikoff AB, Novikoff PM, Rosen OM, Rubin CS (1980) Organelle relationships in cultured 3T3-L1 preadipocytes. J Cell Biol 87:180–196
Pu J, Ha CW, Zhang S, Jung JP, Huh WK, Liu P (2011) Interactomic study on interaction between lipid droplets and mitochondria. Protein Cell 2:487–496
Shaw CS, Jones DA, Wagenmakers AJ (2008) Network distribution of mitochondria and lipid droplets in human muscle fibres. Histochem Cell Biol 129:65–72
Petit JM, Maftah A, Ratinaud MH, Julien R (1992) 10-N nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 209:267–273
Gallet PF, Maftah A, Petit JM, Denis-Gay M, Julien R (1995) Direct cardiolipin assay in yeast using the red fluorescence emission of 10-N-nonyl acridine orange. Eur J Biochem 228:113–119
Jacobson J, Duchen MR, Heales SJ (2002) Intracellular distribution of the fluorescent dye nonyl acridine orange responds to the mitochondrial membrane potential: implications for assays of cardiolipin and mitochondrial mass. J Neurochem 82:224–233
Mileykovskaya E, Dowhan W, Birke RL, Zheng D, Lutterodt L, Haines TH (2001) Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces. FEBS Lett 507:187–190
Morita SY, Terada T (2015) Enzymatic measurement of phosphatidylglycerol and cardiolipin in cultured cells and mitochondria. Sci Rep 5:11737
Boumann HA, Gubbens J, Koorengevel MC, Oh CS, Martin CE, Heck AJR, Patton-Vogt J, Henry SA, de Kruijff B, de Kroon AIPM (2006) Depletion of phosphatidylcholine in yeast induces shortening and increased saturation of the lipid acyl chains: evidence for regulation of intrinsic membrane curvature in a eukaryote. Mol Biol Cell 17(2):1006–1017
Flis VV, Fankl A, Ramprecht C, Zellnig G, Leitner E, Hermetter A, Daum G (2015) Phosphatidylcholine supply to peroxisomes of the yeast Saccharomyces cerevisiae. PLoS One 10(8):e0135084
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(45):37301–37309
De Kroon AI (2007) Metabolism of phosphatidylcholine and its implications for lipid acyl chain composition in Saccharomyces cerevisiae. Biochim Biophys Acta 771(3):343–352
Rockenfeller P, Koska M, Pietrocola F, Minois N, Knittelfelder O, Sica V, Franz J, Carmona-Gutierrez D, Kroemer G, Madeo F (2015) Phosphatidylethanolamine positively regulates autophagy and longevity. Cell Death Differ 22:499–508
Broekhuyse RM (1968) Phospholipids in tissues of the eye. I. Isolation, characterization and quantitative analysis by two-dimensional thin-layer chromatography of diacyl and vinyl-ether phospholipids. Biochim Biophys Acta 152(2):307–315
Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407–427
Casilly CD, Reynolds TB (2018) PS, it’s complicated: the roles of phosphatidylserine and phosphatidylethanolamine in the pathogenesis of Candida albicans and other microbial pathogens. J Fungi (Basel) 4(1):E28. https://doi.org/10.3390/jof4010028
Kay JG, Grinstein S (2011) Sensing phosphatidylserine in cellular membranes. Sensors (Basel) 11(2):1744–1755
Nikawa J, Yamashita S (1997) Phosphatidylinositol synthase from yeast. Biochim Biophys Acta 1348(1–2):173–178
De Camilli P, Emr SD, McPherson PS, Novick P (1996) Phosphoinositides as regulators in membrane traffic. Science 271(5255):1533–1539
Strahl T, Hama H, DeWald DB, Thomer J (2005) Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus. J Cell Biol 171(6):967–979
Wera S, Bergsma JCT, Thevelein JM (2001) Phosphoinositides in yeast: genetically tractable signalling. FEMS Yeast Res 1(1):9–13
Idevall-Hagren O, De Camilli P (2015) Detection and manipulation of phosphoinositides. Biochim Biophys Acta 1851(6):736–745
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Letters R (1966) Phospholipids of yeast II. Extraction, isolation and characterisation of yeast phospholipids. Biochim Biophys Acta 116(3):489–499
Faergeman NJ, Feddersen S, Christiansen JK, Larsen MK, Schneiter R, Ungermann C, Mutenda K, Roepstorff P, Knudsen J (2004) Acyl-CoA-binding protein, Acb1p, is required for normal vacuole function and ceramide synthesis in Saccharomyces cerevisiae. Biochem J 380(Pt 3):907–918
Forrester JS, Milne SB, Ivanova PT, Brown HA (2004) Computational lipidomics: a multiplexed analysis of dynamic changes in membrane lipid composition during signal transduction. Mol Pharmacol 65(4):813–821
Wenk MR (2005) The emerging field of lipidomics. Nat Rev Drug Discov 4(7):594–610
Guan XL, Wenk MR (2006) Mass spectrometry-based profiling of phospholipids and sphingolipids in extracts from Saccharomyces cerevisiae. Yeast 23(6):465–477
Anaokar S, Kodali R, Jonik B, Renne MF, Brouwers JFHM, Lager I, deKroon AIPM, Patton-Vogt I (2019) The glycerophosphocholine acyltransferase Gpc1 is part of a phosphatidylcholine (PC)-remodeling pathway that alters PC species in yeast. J Biol Chem 294:1189–1201
Koeberle A, Shindou H, Koeberle SC, Laufer SA, Shimizu T, Werz O (2013) Arachidonoyl-phosphatidylcholine oscillates during the cell cycle and counteracts proliferation by suppressing Akt membrane binding. Proc Natl Acad Sci USA 110(7):2546–2551
Koeberle A, Pergola C, Shindou H, Koeberle SC, Shimizu T, Laufer SA, Werz O (2015) Role of p38 mitogen-activated protein kinase in linking stearoyl-CoA desaturase-1 activity with endoplasmic reticulum homeostasis. FASEB J 29(6):2439–2449
Spickett CM, Pitt AR (2015) Oxidative lipidomics coming of age: advances in analysis of oxidized phospholipids in physiology and pathology. Antioxid Redox Signal 22(18):1646–1666
Aoyagi R, Ikeda K, Isobe Y, Arita M (2017) Comprehensive analyses of oxidized phospholipids using a measured MS/MS spectra library. J Lipid Res 58(11):2229–2237
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Srinivasan, M., Rajasekharan, R. (2020). Insights into Yeast Phospholipid Tra(ffi)cking. In: Prasad, R., Singh, A. (eds) Analysis of Membrane Lipids. Springer Protocols Handbooks. Springer, New York, NY. https://doi.org/10.1007/978-1-0716-0631-5_4
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DOI: https://doi.org/10.1007/978-1-0716-0631-5_4
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