Recent Advances in Ergosterol Biosynthesis and Regulation Mechanisms in Saccharomyces cerevisiae

Wollam J, Antebi A (2011) Sterol regulation of metabolism, homeostasis and development. Annu Rev Biochem 80:885–916. doi:10.1146/annurev-biochem-081308-165917 Tarkowska D, Strnad M (2016) Plant ecdysteroids: plant sterols with intriguing distributions, biological effects and relations to plant hormones. Planta 244:545–555. doi:10.1007/s00425-016-2561-zz Prasad R, Shah AH, Rawal MK (2016) Antifungals: mechanism of action and drug resistance. Adv Exp Med Biol 892:327–349. doi:10.1007/978-3-319-25304-6_14 Beni A, Soki E, Lajtha K, Fekete I (2014) An optimized HPLC method for soil fungal biomass determination and its application to a detritus manipulation study. J Microbiol Methods 103:124–130. doi:10.1016/j.mimet.2014.05.022 Matteo F, Massimo F, Massimo M, Carmela C (2013) The red seaweed Gracilaria gracilisas a multi products source. Mar Drugs 11:3754. doi:10.3390/md11103754 Huang G, Cai W, Xu B (2016) Vitamin D2, ergosterol, and vitamin B2 content in commercially dried mushrooms marketed in China and increased vitamin D2 content following UV-C irradiation. Int J Vitam Nutr Res. doi:10.1024/0300-9831/a000294 Karpova NV, Andryushina VA, Stytsenko TS, Druzhinina AV, Feofanova TD, Kurakov AV (2016) A search for microscopic fungi with directed hydroxylase activity for the synthesis of steroid drugs. Appl Biochem Microbiol 52:316–323. doi:10.1134/S000368381603008X Kobori M, Yoshida M, Ohnishi-Kameyama M, Shinmoto H (2007) Ergosterol peroxide from an edible mushroom suppresses inflammatory responses in RAW264.7 macrophages and growth of HT29 colon adenocarcinoma cells. Br J Pharmacol 150:209–219. doi:10.1038/sj.bjp.0706972 Kitchawalit S, Kanokmedhakul K, Kanokmedhakul S, Soytong K (2014) A new benzyl ester and ergosterol derivatives from the fungus Gymnoascus reessii. Nat Prod Res 28:1045–1051. doi:10.1080/14786419.2014.903478 Dupont S, Lemetais G, Ferreira T, Cayot P, Gervais P, Beney L (2012) Ergosterol biosynthesis: a fungal pathway for life on land? Evolution 66:2961–2968. doi:10.1111/j.1558-5646.2012.01667.x Krumpe K, Frumkin I, Herzig Y, Rimon N, Özbalci C, Brügger B, Rapaport D, Schuldiner M (2012) Ergosterol content specifies targeting of tail-anchored proteins to mitochondrial outer membranes. Mol Biol Cell 23:3927–3935. doi:10.1091/mbc.E11-12-0994 Zhang YQ, Gamarra S, Garciaeffron G, Park S, Perlin DS, Rao R (2010) Requirement for ergosterol in V-ATPase function underlies antifungal activity of azole drugs. PLoS Pathog 6:e1000939. doi:10.1371/journal.ppat.1000939 Choudhary V, Schneiter R (2012) Pathogen-Related Yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins. Proc Natl Acad Sci USA 109:16882–16887. doi:10.1073/pnas.1209086109 Malik P, Chaudhry N, Kitawat SB, Kumar R, Mukherjee T (2014) Relationship of azole resistance with the structural alteration of the target sites: novel synthetic compounds for better antifungal activities. Nat Prod J 4:131–139. doi:10.2174/221031550402141009100455 Aguilera F, Peinado RA, Millán C, Ortega JM, Mauricio JC (2006) Relationship between ethanol tolerance, H+-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. Int J Food Microbiol 110:34–42. doi:10.1016/j.ijfoodmicro.2006.02.002 Inoue T, Iefuji H, Fujii T, Soga H, Satoh K (2000) Cloning and characterization of a gene complementing the mutation of an ethanol-sensitive mutant of sake yeast. Biosci Biotechnol Biochem 64:229–236. doi:10.1271/bbb.64.229 Henderson CM, Block DE (2014) Examining the role of membrane lipid composition in determining the ethanol tolerance of saccharomyces cerevisiae. Appl Environ Microbiol 80:2966. doi:10.1128/AEM.04151-13 Kamthan A, Kamthan M, Datta A (2017) Expression of C-5 sterol desaturase from an edible mushroom in fisson yeast enhances its ethanol and thermotolerance. PLoS ONE 12:e0173381. doi:10.1371/journal.pone.0173381 Kodedová M, Sychrová H (2015) Changes in the sterol composition of the plasma membrane affect membrane potential, salt tolerance and the activity of multidrug resistance pumps in Saccharomyces cerevisiae. PLoS ONE 10:e0139306. doi:10.1371/journal.pone.0139306 Montañés FM, Pascual-Ahuir A, Proft M (2011) Repression of ergosterol biosynthesis is essential for stress resistance and is mediated by the Hog1 MAP kinase and the Mot3 and Rox1 transcription factors. Mol Microbiol 79:1008–1023. doi:10.1111/j.1365-2958.2010.07502.x Marisco G, Saito ST, Ganda IS, Brendel M, Pungartnik C (2011) Low ergosterol content in yeast adh 1 mutant enhances chitin maldistribution and sensitivity to paraquat-induced oxidative stress. Yeast 28:363–373. doi:10.1002/yea.1844 Landolfo S, Zara G, Zara S, Budroni M, Ciani M, Mannazzu I (2010) Oleic acid and ergosterol supplementation mitigates oxidative stress in wine strains of Saccharomyces cerevisiae. Int J Food Microbiol 141:229–235. doi:10.1016/j.ijfoodmicro.2010.05.020 Liu J, Zhu Y, Du G, Zhou J, Chen J (2013) Exogenous ergosterol protects Saccharomyces cerevisiae from d -limonene stress. J Appl Microbiol 114:482–491. doi:10.1111/jam.12046 Davies BS, Rine J (2006) A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 174:191–201. doi:10.1534/genetics.106.059964 Kishimoto T, Yamamoto T, Tanaka K (2005) Defects in structural integrity of ergosterol and the cdc50p-drs2p putative phospholipid translocase cause accumulation of endocytic membranes, onto which actin patches are assembled in yeast. Mol Biol Cell 16:5592–5609. doi:10.1091/mbc.E05-05-0452 Miziorko HM (2011) Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch Biochem Biophys 505:131–143. doi:10.1016/j.abb.2010.09.028 Klug L, Daum G (2014) Yeast lipid metabolism at a glance. FEMS Yeast Res 14:369–388. doi:10.1111/1567-1364.12141 Hayakawa H, Sobue F, Motoyama K et al (2017) Identification of enzymes involved in the mevalonate pathway of Flavobacterium johnsoniae. Biochem Biophys Res Commun 487:702–708. doi:10.1016/j.bbrc.2017.04.120 Lee SH, Raboune S, Walker JM, Bradshaw HB (2010) Distribution of endogenous farnesyl pyrophosphate and four species of lysophosphatidic acid in rodent brain. Int J Mol Sci 11:3965–3976. doi:10.3390/ijms11103965 Kristan K, Rizner TL (2012) Steroid-transforming enzymes in fungi. J Steroid Biochem Mol Biol 129:79–91. doi:10.1016/j.jsbmb.2011.08.012 Konecna A, Toth Hervay N, Valachovic M, Gbelska Y (2016) ERG6 gene deletion modifies Kluyveromyces lactis susceptibility to various growth inhibitors. Yeast 33:621–632. doi:10.1002/yea.3212 Mo C, Bard M (2005) Erg28p is a key protein in the yeast sterol biosynthetic enzyme complex. J Lipid Res 46:1991–1998. doi:10.1073/pnas.112202799 Clay L, Caudron F, Denothlippuner A, Boettcher B, Frei SB, Snapp EL, Barral Y (2014) A sphingolipid-dependent diffusion barrier confines ER stress to the yeast mother cell. Elife 3:e01883. doi:10.7554/eLife.01883 Kodedova M, Sychrova H (2015) Changes in the sterol composition of the plasma membrane affect membrane potential, salt tolerance and the activity of multidrug resistance pumps in Saccharomyces cerevisiae. PLoS ONE 10:e0139306. doi:10.1371/journal.pone.0139306 Espenshade PJ, Hughes AL (2007) Regulation of sterol synthesis in eukaryotes. Annu Rev Genet 41:401–427. doi:10.1146/annurev.genet.41.110306.130315 Burg JS, Espenshade PJ (2011) Regulation of HMG-CoA reductase in mammals and yeast. Prog Lipid Res 50:403–410. doi:10.1016/j.plipres.2011.07.002 Foresti O, Ruggiano A, Hannibalbach HK, Ejsing CS, Carvalho P (2012) Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. Elife 2:1600–1613. doi:10.7554/eLife.00953 Dhingra S, Cramer RA (2017) Regulation of sterol biosynthesis in the human fungal pathogen Aspergillus fumigatus: opportunities for therapeutic development. Front Microbiol. doi:10.3389/fmicb.2017.00092 Zavrel M, Hoot SJ, White TC (2013) Comparison of sterol import under aerobic and anaerobic conditions in three fungal species, Candida albicans, Candida glabrata, and Saccharomyces cerevisiae. Eukaryot Cell 12:725–738. doi:10.1128/EC.00345-12 Shakouryelizeh M, Protchenko O, Berger A, Cox J, Gable K, Dunn TM, Prinz WA, Bard M, Philpott CC (2010) Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem 285:14823–14833. doi:10.1074/jbc.M109.091710 Puig S, Askeland E, Thiele JD (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120:99. doi:10.1016/j.cell.2004.11.032 Craven RJ, Mallory JC, Hand RA (2007) Regulation of iron homeostasis mediated by the heme-binding protein Dap1 (damage resistance protein 1) via the P450 protein Erg11/Cyp51. J Biol Chem 282:36543–36551. doi:10.1074/jbc.M706770200 Layer JV, Barnes BM, Yamasaki Y, Barbuch R, Li L, Taramino S, Balliano G, Bard M (2013) Characterization of a mutation that results in independence of oxidosqualene cyclase (Erg7) activity from the downstream 3-ketoreductase (Erg27) in the yeast ergosterol biosynthetic pathway. Biochim Biophys Acta 1831:361–369. doi:10.1016/j.bbalip.2012.09.012 Luna-Tapia A, Peters BM, Eberle KE, Kerns ME, Foster TP, Marrero L, Noverr MC, Fidel PL Jr, Palmer GE (2015) ERG2 and ERG24 are required for normal vacuolar physiology as well as Candida albicans pathogenicity in a murine model of disseminated but not vaginal candidiasis. Eukaryot Cell 14:1006–1016. doi:10.1128/EC.00116-15 Náhlík J, Hrnčiřík P, Mareš J, Rychtera M, Kent CA (2017) Towards the design of an optimal strategy for the production of ergosterol from Saccharomyces cerevisiae yeasts. Biotechnol Progr. doi:10.1002/btpr.2436 Ploier B, Korber M, Schmidt C, Koch B, Leitner E, Daum G (2015) Regulatory link between steryl ester formation and hydrolysis in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1851:977–986. doi:10.1016/j.bbalip.2015.02.011 Grillitsch K, Connerth M, Köfeler H, Arrey TN, Rietschel B, Wagner B, Karas M, Daum G (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: lipidome meets proteome. Biochim Biophys Acta 1811:1165–1176. doi:10.1016/j.bbalip.2011.07.015 Sorger D, Athenstaedt K, Hrastnik C, Daum G (2004) A yeast strain lacking lipid particles bears a defect in ergosterol formation. J Biol Chem 279:31190–31196. doi:10.1074/jbc.M403251200 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. doi:10.1038/sj.emboj.7601924 Sullivan DP, Ohvorekilä H, Baumann NA, Beh CT, Menon AK (2006) Sterol trafficking between the endoplasmic reticulum and plasma membrane in yeast. Biochem Soc Trans 34:356–358. doi:10.1042/BST0340356 Jacquier N, Schneiter R (2012) Mechanisms of sterol uptake and transport in yeast. J Steroid Biochem Mol Biol 129:70–78. doi:10.1016/j.jsbmb.2010.11.014 Perry RJ, Ridgway ND (2006) Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein. Mol Biol Cell 17:2604–2616. doi:10.1091/mbc.E06-01-0060 Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) osh proteins regulate phosphoinositide metabolism at er-plasma membrane contact sites. Cell 144:389–401 Schulz TA, Prinz WA (2007) Sterol transport in yeast and the oxysterol binding protein homologue (OSH) family. Biochim Biophys Acta 1771:769–780. doi:10.1016/j.bbalip.2007.03.003 Leblanc MA, Fairn GD, Russo SB, Czyz O, Zaremberg V, Cowart LA, Mcmaster CR (2013) The yeast oxysterol binding protein Kes1 maintains sphingolipid levels. PLoS ONE 8:e60485. doi:10.1371/journal.pone.0060485 Tong F, Billheimer J, Shechtman CF, Liu Y, Crooke R, Graham M, Cohen DE, Sturley SL, Rader DJ (2010) Decreased expression of ARV1 results in cholesterol retention in the endoplasmic reticulum and abnormal bile acid metabolism. J Biol Chem 285:33632–33641. doi:10.1074/jbc.M110.165761 Ruggles KV, Garbarino J, Liu Y, Moon J, Schneider K, Henneberry A, Billheimer J, Millar JS, Marchadier D, Valasek MA (2014) A functional, genome-wide evaluation of liposensitive yeast identifies the “ARE2 required for viability” (ARV1) gene product as a major component of eukaryotic fatty acid resistance. J Biol Chem 289:4417–4431. doi:10.1074/jbc.M113.515197 Munkacsi AB, Porto AF, Sturley SL (2007) Niemann–Pick type C disease proteins: orphan transporters or membrane rheostats? Future Lipidol 2:357–367. doi:10.2217/17460875.2.3.357 Malathi K, Higaki K, Tinkelenberg AH, Balderes DA, Almanzar-Paramio D, Wilcox LJ, Erdeniz N, Redican F, Padamsee M, Liu Y (2004) Mutagenesis of the putative sterol-sensing domain of yeast Niemann Pick C-related protein reveals a primordial role in subcellular sphingolipid distribution. J Cell Biol 164:547–556. doi:10.1083/jcb.200310046 Zhang S, Ren J, Li H, Zhang Q, Armstrong JS, Munn AL, Yang H (2004) Ncr1p, the yeast ortholog of mammalian Niemann Pick C1 protein, is dispensable for endocytic transport. Traffic 5:1017–1030. doi:10.1111/j.1600-0854.2004.00241.x Berger AC, Vanderford TH, Gernert KM, Nichols JW, Faundez V, Corbett AH (2005) Saccharomyces cerevisiae Npc2p is a functionally conserved homologue of the human Niemann-Pick disease type C 2 protein, hNPC2. Eukaryot Cell 4:1851–1862. doi:10.1128/EC.4.11.1851-1862.2005 Zhang Ke, Tong Mengmeng, Gao Kehui, Di Yanan, Wang Pinmei, Zhang Chunfang, Wu Xuechang, Zheng Daoqiong (2015) Genomic reconstruction to improve bioethanol and ergosterol production of industrial yeast Saccharomyces cerevisiae. J Ind Microbiol Biot 42:207–218. doi:10.1007/s10295-014-1556-7 Wriessnegger T, Pichler H (2013) Yeast metabolic engineering–targeting sterol metabolism and terpenoid formation. Prog Lipid Res 52:277–293. doi:10.1016/j.plipres.2013.03.001 Paramasivan K, Mutturi S (2017) Progress in terpene synthesis strategies through engineering of Saccharomyces cerevisiae. Crit Rev Biotechnol. doi:10.1080/07388551.2017.1299679