CoChat
Sign Up
Cited by 65Lipid metabolism and biosynthesisCancer, Lipids, and MetabolismAutophagy in Disease and Therapy

Lipid droplet‐mediated lipid and protein homeostasis in budding yeast

Open access
Graef, Martin·2018·FEBS Letters
DOI 10.1002/1873-3468.12996PMC PMC5947121
Open this paper in CoChat — free accountOpen PDF

Abstract

Lipid droplets are conserved specialized organelles that store neutral lipids. Our view on this unique organelle has evolved from a simple fat deposit to a highly dynamic and functionally diverse hub-one that mediates the buffering of fatty acid stress and the adaptive reshaping of lipid metabolism to promote membrane and organelle homeostasis and the integrity of central proteostasis pathways, including autophagy, which ensure stress resistance and cell survival. This Review will summarize the recent developments in the budding yeast Saccharomyces cerevisiae, as this model organism has been instrumental in deciphering the fundamental mechanisms and principles of lipid droplet biology and interconnecting lipid droplets with many unanticipated cellular functions applicable to many other cell systems.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1002/1873-3468.12996

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 111

  1. [1]Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249, 541– 585. 22002710
  2. [2]Choudhary V, Ojha N, Golden A and Prinz WA (2015) A conserved family of proteins facilitates nascent lipid droplet budding from the ER. J Cell Biol 211, 261– 271. 26504167 PMC4621845
  3. [3]Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F and Schneiter R (2011) Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Sci 124, 2424– 2437. 21693588
  4. [4]Mishra S, Khaddaj R, Cottier S, Stradalova V, Jacob C and Schneiter R (2016) Mature lipid droplets are accessible to ER luminal proteins. J Cell Sci 129, 3803– 3815. 27591256
  5. [5]Hariri H, Rogers S, Ugrankar R, Liu YL, Feathers JR and Henne WM (2017) Lipid droplet biogenesis is spatially coordinated at ER‐vacuole contacts under nutritional stress. EMBO Rep 19, 57– 72. 29146766 PMC5757283
  6. [6]Carter JR and Kennedy EP (1966) Enzymatic synthesis of cytidine diphosphate diglyceride. J Lipid Res 7, 678– 683. 4291255
  7. [7]Kelley MJ and Carman GM (1987) Purification and characterization of CDP‐diacylglycerol synthase from Saccharomyces cerevisiae. J Biol Chem 262, 14563– 14570. 2822695
  8. [8]Shen H, Heacock PN, Clancey CJ and Dowhan W (1996) The CDS1 gene encoding CDP‐diacylglycerol synthase in Saccharomyces cerevisiae is essential for cell growth. J Biol Chem 271, 789– 795. 8557688
  9. [9]Henry SA, Kohlwein SD and Carman GM (2012) Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics 190, 317– 349. 22345606 PMC3276621
  10. [10]Han GS, Wu WI and Carman GM (2006) The Saccharomyces cerevisiae Lipin homolog is a Mg2 + ‐dependent phosphatidate phosphatase enzyme. J Biol Chem 281, 9210– 9218. 16467296 PMC1424669
  11. [11]He Y, Yam C, Pomraning K, Chin JS, Yew JY, Freitag M and Oliferenko S (2014) Increase in cellular triacylglycerol content and emergence of large ER‐associated lipid droplets in the absence of CDP‐DG synthase function. Mol Biol Cell 25, 4083– 4095. 25318672 PMC4263451
  12. [12]Su WM, Han GS and Carman GM (2014) Yeast Nem1‐Spo7 protein phosphatase activity on Pah1 phosphatidate phosphatase is specific for the Pho85‐Pho80 protein kinase phosphorylation sites. J Biol Chem 289, 34699– 34708. 25359770 PMC4263874
  13. [13]Hsieh LS, Su WM, Han GS and Carman GM (2016) Phosphorylation of yeast Pah1 phosphatidate phosphatase by casein kinase II regulates its function in lipid metabolism. J Biol Chem 291, 9974– 9990. 27044741 PMC4859001
  14. [14]Choi HS, Su WM, Morgan JM, Han GS, Xu Z, Karanasios E, Siniossoglou S and Carman GM (2011) Phosphorylation of phosphatidate phosphatase regulates its membrane association and physiological functions in Saccharomyces cerevisiae: identification of SER(602), THR(723), AND SER(744) as the sites phosphorylated by CDC28 (CDK1)‐encoded cyclin‐dependent kinase. J Biol Chem 286, 1486– 1498. 21081492 PMC3020757
  15. [15]Choi HS, Su WM, Han GS, Plote D, Xu Z and Carman GM (2012) Pho85p‐Pho80p phosphorylation of yeast Pah1p phosphatidate phosphatase regulates its activity, location, abundance, and function in lipid metabolism. J Biol Chem 287, 11290– 11301. 22334681 PMC3322823
  16. [16]Su WM, Han GS, Casciano J and Carman GM (2012) Protein kinase A‐mediated phosphorylation of Pah1p phosphatidate phosphatase functions in conjunction with the Pho85p‐Pho80p and Cdc28p‐cyclin B kinases to regulate lipid synthesis in yeast. J Biol Chem 287, 33364– 33376. 22865862 PMC3460439
  17. [17]Karanasios E, Han GS, Xu Z, Carman GM and Siniossoglou S (2010) A phosphorylation‐regulated amphipathic helix controls the membrane translocation and function of the yeast phosphatidate phosphatase. Proc Natl Acad Sci USA 107, 17539– 17544. 20876142 PMC2955120
  18. [18]Siniossoglou S, Santos‐Rosa H, Rappsilber J, Mann M and Hurt E (1998) A novel complex of membrane proteins required for formation of a spherical nucleus. EMBO J 17, 6449– 6464. 9822591 PMC1170993
  19. [19]Santos‐Rosa H, Leung J, Grimsey N, Peak‐Chew S and Siniossoglou S (2005) The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J 24, 1931– 1941. 15889145 PMC1142606
  20. [20]Dubots E, Cottier S, Peli‐Gulli MP, Jaquenoud M, Bontron S, Schneiter R and De Virgilio C (2014) TORC1 regulates Pah1 phosphatidate phosphatase activity via the Nem1/Spo7 protein phosphatase complex. PLoS One 9, e104194. 25117580 PMC4130541
  21. [21]Fakas S, Qiu Y, Dixon JL, Han GS, Ruggles KV, Garbarino J, Sturley SL and Carman GM (2011) Phosphatidate phosphatase activity plays key role in protection against fatty acid‐induced toxicity in yeast. J Biol Chem 286, 29074– 29085. 21708942 PMC3190715
  22. [22]Barbosa AD, Sembongi H, Su WM, Abreu S, Reggiori F, Carman GM and Siniossoglou S (2015) Lipid partitioning at the nuclear envelope controls membrane biogenesis. Mol Biol Cell 26, 3641– 3657. 26269581 PMC4603934
  23. [23]Adeyo O, Horn PJ, Lee S, Binns DD, Chandrahas A, Chapman KD and Goodman JM (2011) The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J Cell Biol 192, 1043– 1055. 21422231 PMC3063132
  24. [24]Han GS, O'Hara L, Carman GM and Siniossoglou S (2008) An unconventional diacylglycerol kinase that regulates phospholipid synthesis and nuclear membrane growth. J Biol Chem 283, 20433– 20442. 18458075 PMC2459266
  25. [25]Han GS, O'Hara L, Siniossoglou S and Carman GM (2008) Characterization of the yeast DGK1‐encoded CTP‐dependent diacylglycerol kinase. J Biol Chem 283, 20443– 20453. 18458076 PMC2459283
  26. [26]Stone SJ, Levin MC and Farese RV Jr (2006) Membrane topology and identification of key functional amino acid residues of murine acyl‐CoA:diacylglycerol acyltransferase‐2. J Biol Chem 281, 40273– 40282. 17035227
  27. [27]Oelkers P, Cromley D, Padamsee M, Billheimer JT and Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277, 8877– 8881. 11751875
  28. [28]Sorger D and Daum G (2002) Synthesis of triacylglycerols by the acyl‐coenzyme A:diacyl‐glycerol acyltransferase Dga1p in lipid particles of the yeast Saccharomyces cerevisiae. J Bacteriol 184, 519– 524. 11751830 PMC139573
  29. [29]Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H and 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 USA 97, 6487– 6492. 10829075 PMC18631
  30. [30]Horvath SE, Wagner A, Steyrer E and Daum G (2011) Metabolic link between phosphatidylethanolamine and triacylglycerol metabolism in the yeast Saccharomyces cerevisiae. Biochem Biophys Acta 1811, 1030– 1037. 21875690 PMC3229975
  31. [31]Athenstaedt K, Zweytick D, Jandrositz A, Kohlwein SD and Daum G (1999) Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J Bacteriol 181, 6441– 6448. 10515935 PMC103780
  32. [32]Oelkers P, Tinkelenberg A, Erdeniz N, Cromley D, Billheimer JT and Sturley SL (2000) A lecithin cholesterol acyltransferase‐like gene mediates diacylglycerol esterification in yeast. J Biol Chem 275, 15609– 15612. 10747858
  33. [33]Zweytick D, Leitner E, Kohlwein SD, Yu C, Rothblatt J and Daum G (2000) Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae. Eur J Biochem 267, 1075– 1082. 10672016
  34. [34]Yang H, Bard M, Bruner DA, Gleeson A, Deckelbaum RJ, Aljinovic G, Pohl TM, Rothstein R and Sturley SL (1996) Sterol esterification in yeast: a two‐gene process. Science 272, 1353– 1356. 8650549
  35. [35]Yu C, Kennedy NJ, Chang CC and Rothblatt JA (1996) Molecular cloning and characterization of two isoforms of Saccharomyces cerevisiae acyl‐CoA:sterol acyltransferase. J Biol Chem 271, 24157– 24163. 8798656
  36. [36]Sandager L, Dahlqvist A, Banas A, Stahl U, Lenman M, Gustavsson M and Stymne S (2000) An acyl‐CoA:cholesterol acyltransferase (ACAT)‐related gene is involved in the accumulation of triacylglycerols in Saccharomyces cerevisiae. Biochem Soc Trans 28, 700– 702. 11171176
  37. [37]Sandager L, Gustavsson MH, Stahl U, Dahlqvist A, Wiberg E, Banas A, Lenman M, Ronne H and Stymne S (2002) Storage lipid synthesis is non‐essential in yeast. J Biol Chem 277, 6478– 6482. 11741946
  38. [38]Binns D, Lee S, Hilton CL, Jiang QX and Goodman JM (2010) Seipin is a discrete homooligomer. Biochemistry 49, 10747– 10755. 21062080 PMC3086013
  39. [39]Wang CW, Miao YH and Chang YS (2014) Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16. J Cell Sci 127, 1214– 1228. 24434579
  40. [40]Szymanski KM, Binns D, Bartz R, Grishin NV, Li WP, Agarwal AK, Garg A, Anderson RG and 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 USA 104, 20890– 20895. 18093937 PMC2409237
  41. [41]Fei W, Shui G, Gaeta B, Du X, Kuerschner L, Li P, Brown AJ, Wenk MR, Parton RG and Yang H (2008) Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J Cell Biol 180, 473– 482. 18250201 PMC2234226
  42. [42]Cartwright BR, Binns DD, Hilton CL, Han S, Gao Q and Goodman JM (2015) Seipin performs dissectible functions in promoting lipid droplet biogenesis and regulating droplet morphology. Mol Biol Cell 26, 726– 739. 25540432 PMC4325842
  43. [43]Fei W, Shui G, Zhang Y, Krahmer N, Ferguson C, Kapterian TS, Lin RC, Dawes IW, Brown AJ, Li P et al (2011) A role for phosphatidic acid in the formation of “supersized” lipid droplets. PLoS Genet 7, e1002201. 21829381 PMC3145623
  44. [44]Wolinski H, Hofbauer HF, Hellauer K, Cristobal‐Sarramian A, Kolb D, Radulovic M, Knittelfelder OL, Rechberger GN and Kohlwein SD (2015) Seipin is involved in the regulation of phosphatidic acid metabolism at a subdomain of the nuclear envelope in yeast. Biochem Biophys Acta 1851, 1450– 1464. 26275961
  45. [45]Wolinski H, Kolb D, Hermann S, Koning RI and Kohlwein SD (2011) A role for seipin in lipid droplet dynamics and inheritance in yeast. J Cell Sci 124, 3894– 3904. 22100922
  46. [46]Grippa A, Buxo L, Mora G, Funaya C, Idrissi FZ, Mancuso F, Gomez R, Muntanya J, Sabido E and Carvalho P (2015) The seipin complex Fld1/Ldb16 stabilizes ER‐lipid droplet contact sites. J Cell Biol 211, 829– 844. 26572621 PMC4657162
  47. [47]Teixeira V, Johnsen L, Martinez‐Montanes F, Grippa A, Buxo L, Idrissi FZ, Ejsing CS and Carvalho P (2017) Regulation of lipid droplets by metabolically controlled Ldo isoforms. J Cell Biol 217, 127– 138. 29187528 PMC5748980
  48. [48]Ren J, Pei‐Chen Lin C, Pathak MC, Temple BR, Nile AH, Mousley CJ, Duncan MC, Eckert DM, Leiker TJ, Ivanova PT et al (2014) A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress‐induced membrane biogenesis. Mol Biol Cell 25, 712– 727. 24403601 PMC3937096
  49. [49]Eisenberg‐Bord M, Mari M, Weill U, Rosenfeld‐Gur E, Moldavski O, Castro IG, Soni KG, Harpaz N, Levine TP, Futerman AH et al (2017) Identification of seipin‐linked factors that act as determinants of a lipid droplet subpopulation. J Cell Biol 217, 269– 282. 29187527 PMC5748981
  50. [50]Selitrennik M and Lev S (2016) The role of phosphatidylinositol‐transfer proteins at membrane contact sites. Biochem Soc Trans 44, 419– 424. 27068949
  51. [51]Moir RD, Gross DA, Silver DL and Willis IM (2012) SCS3 and YFT2 link transcription of phospholipid biosynthetic genes to ER stress and the UPR. PLoS Genet 8, e1002890. 22927826 PMC3426550
  52. [53]Gross DA, Zhan C and Silver DL (2011) Direct binding of triglyceride to fat storage‐inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proc Natl Acad Sci USA 108, 19581– 19586. 22106267 PMC3241795
  53. [54]Gao Q, Binns DD, Kinch LN, Grishin NV, Ortiz N, Chen X and Goodman JM (2017) Pet10p is a yeast perilipin that stabilizes lipid droplets and promotes their assembly. J Cell Biol 216, 3199– 3217. 28801319 PMC5626530
  54. [55]Athenstaedt K and Daum G (2003) YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J Biol Chem 278, 23317– 23323. 12682047
  55. [56]Athenstaedt K and 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. 16135509
  56. [57]Ploier B, Scharwey M, Koch B, Schmidt C, Schatte J, Rechberger G, Kollroser M, Hermetter A and Daum G (2013) Screening for hydrolytic enzymes reveals Ayr1p as a novel triacylglycerol lipase in Saccharomyces cerevisiae. J Biol Chem 288, 36061– 36072. 24187129 PMC3861654
  57. [58]Debelyy MO, Thoms S, Connerth M, Daum G and Erdmann R (2011) Involvement of the Saccharomyces cerevisiae hydrolase Ldh1p in lipid homeostasis. Eukaryot Cell 10, 776– 781. 21478434 PMC3127674
  58. [59]Thoms S, Debelyy MO, Connerth M, Daum G and Erdmann R (2011) The putative Saccharomyces cerevisiae hydrolase Ldh1p is localized to lipid droplets. Eukaryot Cell 10, 770– 775. 21478430 PMC3127662
  59. [60]Rajakumari S and Daum G (2010) Janus‐faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21, 501– 510. 20016004 PMC2820416
  60. [61]Rajakumari S and Daum G (2010) Multiple functions as lipase, steryl ester hydrolase, phospholipase, and acyltransferase of Tgl4p from the yeast Saccharomyces cerevisiae. J Biol Chem 285, 15769– 15776. 20332534 PMC2871444
  61. [62]Schmidt C, Athenstaedt K, Koch B, Ploier B and Daum G (2013) Regulation of the yeast triacylglycerol lipase TGl3p by formation of nonpolar lipids. J Biol Chem 288, 19939– 19948. 23673660 PMC3707694
  62. [63]Koch B, Schmidt C, Ploier B and Daum G (2014) Modifications of the C terminus affect functionality and stability of yeast triacylglycerol lipase Tgl3p. J Biol Chem 289, 19306– 19316. 24847060 PMC4094043
  63. [64]Klein I, Klug L, Schmidt C, Zandl M, Korber M, Daum G and 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. 27170177 PMC4927276
  64. [65]Heier C, Taschler U, Rengachari S, Oberer M, Wolinski H, Natter K, Kohlwein SD, Leber R and Zimmermann R (2010) Identification of Yju3p as functional orthologue of mammalian monoglyceride lipase in the yeast Saccharomycescerevisiae. Biochem Biophys Acta 1801, 1063– 1071. 20554061 PMC2911655
  65. [66]Vishnu Varthini L, Selvaraju K, Srinivasan M and Nachiappan V (2015) ROG1 encodes a monoacylglycerol lipase in Saccharomyces cerevisiae. FEBS Lett 589, 23– 30. 25433290
  66. [67]Selvaraju K, Gowsalya R, Vijayakumar R and Nachiappan V (2016) MGL2/YMR210w encodes a monoacylglycerol lipase in Saccharomyces cerevisiae. FEBS Lett 590, 1174– 1186. 26991558
  67. [68]Koffel R, Tiwari R, Falquet L and 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. 15713625 PMC549362
  68. [69]Mullner H, Deutsch G, Leitner E, Ingolic E and Daum G (2005) YEH2/YLR020c encodes a novel steryl ester hydrolase of the yeast Saccharomyces cerevisiae. J Biol Chem 280, 13321– 13328. 15632184
  69. [70]Jandrositz A, Petschnigg J, Zimmermann R, Natter K, Scholze H, Hermetter A, Kohlwein SD and Leber R (2005) The lipid droplet enzyme Tgl1p hydrolyzes both steryl esters and triglycerides in the yeast, Saccharomyces cerevisiae. Biochem Biophys Acta 1735, 50– 58. 15922657
  70. [71]Klein I, Korber M, Athenstaedt K and Daum G (2017) The impact of nonpolar lipids on the regulation of the steryl ester hydrolases Tgl1p and Yeh1p in the yeast Saccharomyces cerevisiae. Biochem Biophys Acta 1862, 1491– 1501. 28866104
  71. [72]Fakas S, Konstantinou C and Carman GM (2011) DGK1‐encoded diacylglycerol kinase activity is required for phospholipid synthesis during growth resumption from stationary phase in Saccharomyces cerevisiae. J Biol Chem 286, 1464– 1474. 21071438 PMC3020755
  72. [73]Kuchler K, Daum G and Paltauf F (1986) Subcellular and submitochondrial localization of phospholipid‐synthesizing enzymes in Saccharomyces cerevisiae. J Bacteriol 165, 901– 910. 3005242 PMC214514
  73. [74]Markgraf DF, Klemm RW, Junker M, Hannibal‐Bach HK, Ejsing CS and Rapoport TA (2014) An ER protein functionally couples neutral lipid metabolism on lipid droplets to membrane lipid synthesis in the ER. Cell Rep 6, 44– 55. 24373967 PMC3947819
  74. [75]Petschnigg J, Wolinski H, Kolb D, Zellnig G, Kurat CF, Natter K and Kohlwein SD (2009) Good fat, essential cellular requirements for triacylglycerol synthesis to maintain membrane homeostasis in yeast. J Biol Chem 284, 30981– 30993. 19608739 PMC2781499
  75. [76]Suzuki K, Kubota Y, Sekito T and Ohsumi Y (2007) Hierarchy of Atg proteins in pre‐autophagosomal structure organization. Genes Cells 12, 209– 218. 17295840
  76. [78]Kraft C and Martens S (2012) Mechanisms and regulation of autophagosome formation. Curr Opin Cell Biol 24, 496– 501. 22664348
  77. [79]Lamb CA, Yoshimori T and Tooze SA (2013) The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14, 759– 774. 24201109
  78. [80]Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM and Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458, 1131– 1135. 19339967 PMC2676208
  79. [81]Tsuji T, Fujimoto M, Tatematsu T, Cheng J, Orii M, Takatori S & Fujimoto T. (2017) Niemann‐Pick type C proteins promote microautophagy by expanding raft‐like membrane domains in the yeast vacuole. eLife 6, e25960. 28590904 PMC5462540
  80. [82]Wang CW, Miao YH and Chang YS (2014) A sterol‐enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast. J Cell Biol 206, 357– 366. 25070953 PMC4121974
  81. [83]van Zutphen T, Todde V, de Boer R, Kreim M, Hofbauer HF, Wolinski H, Veenhuis M, van der Klei IJ and Kohlwein SD (2014) Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol Biol Cell 25, 290– 301. 24258026 PMC3890349
  82. [84]Vevea JD, Garcia EJ, Chan RB, Zhou B, Schultz M, Di Paolo G, McCaffery JM and Pon LA (2015) Role for Lipid Droplet Biogenesis and Microlipophagy in Adaptation to Lipid Imbalance in Yeast. Dev Cell 35, 584– 599. 26651293 PMC4679156
  83. [85]Seo AY, Lau PW, Feliciano D, Sengupta P, Gros MAL, Cinquin B, Larabell CA and Lippincott‐Schwartz J (2017) AMPK and vacuole‐associated Atg14p orchestrate mu‐lipophagy for energy production and long‐term survival under glucose starvation. eLife 6, e21690. 28394250 PMC5407857
  84. [86]Uttenweiler A and Mayer A (2008) Microautophagy in the yeast Saccharomyces cerevisiae. Methods Mol Biol 445, 245– 259. 18425455
  85. [87]Toulmay A and Prinz WA (2013) Direct imaging reveals stable, micrometer‐scale lipid domains that segregate proteins in live cells. J Cell Biol 202, 35– 44. 23836928 PMC3704982
  86. [88]Oku M, Maeda Y, Kagohashi Y, Kondo T, Yamada M, Fujimoto T and Sakai Y (2017) Evidence for ESCRT‐ and clathrin‐dependent microautophagy. J Cell Biol 216, 3263– 3274. 28838958 PMC5626533
  87. [89]Olzmann JA and Kopito RR (2011) Lipid droplet formation is dispensable for endoplasmic reticulum‐associated degradation. J Biol Chem 286, 27872– 27874. 21693705 PMC3151032
  88. [90]Velazquez AP, Tatsuta T, Ghillebert R, Drescher I and Graef M (2016) Lipid droplet‐mediated ER homeostasis regulates autophagy and cell survival during starvation. J Cell Biol 212, 621– 631. 26953354 PMC4792078
  89. [91]Connerth M, Czabany T, Wagner A, Zellnig G, Leitner E, Steyrer E and Daum G (2010) Oleate inhibits steryl ester synthesis and causes liposensitivity in yeast. J Biol Chem 285, 26832– 26841. 20571028 PMC2930682
  90. [92]Garbarino J, Padamsee M, Wilcox L, Oelkers PM, D'Ambrosio D, Ruggles KV, Ramsey N, Jabado O, Turkish A and Sturley SL (2009) Sterol and diacylglycerol acyltransferase deficiency triggers fatty acid‐mediated cell death. J Biol Chem 284, 30994– 31005. 19690167 PMC2781500
  91. [93]Shpilka T, Welter E, Borovsky N, Amar N, Mari M, Reggiori F and Elazar Z (2015) Lipid droplets and their component triglycerides and steryl esters regulate autophagosome biogenesis. EMBO J 34, 2117– 2131. 26162625 PMC4557665
  92. [94]Li D, Song JZ, Li H, Shan MH, Liang Y, Zhu J and Xie Z (2015) Storage lipid synthesis is necessary for autophagy induced by nitrogen starvation. FEBS Lett 589, 269– 276. 25500271
  93. [95]Moldavski O, Amen T, Levin‐Zaidman S, Eisenstein M, Rogachev I, Brandis A, Kaganovich D and Schuldiner M (2015) Lipid droplets are essential for efficient clearance of cytosolic inclusion bodies. Dev Cell 33, 603– 610. 26004510
  94. [96]Ruggles KV, Garbarino J, Liu Y, Moon J, Schneider K, Henneberry A, Billheimer J, Millar JS, Marchadier D, Valasek MA et al (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. 24273168 PMC3924304
  95. [97]Stukey JE, McDonough VM and Martin CE (1989) Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J Biol Chem 264, 16537– 16544. 2674136
  96. [98]Stukey JE, McDonough VM and Martin CE (1990) The OLE1 gene of Saccharomyces cerevisiae encodes the delta 9 fatty acid desaturase and can be functionally replaced by the rat stearoyl‐CoA desaturase gene. J Biol Chem 265, 20144– 20149. 1978720
  97. [99]Mitchell AG and Martin CE (1995) A novel cytochrome b5‐like domain is linked to the carboxyl terminus of the Saccharomyces cerevisiae delta‐9 fatty acid desaturase. J Biol Chem 270, 29766– 29772. 8530368
  98. [100]Ballweg S and Ernst R (2017) Control of membrane fluidity: the OLE pathway in focus. Biol Chem 398, 215– 228. 27787227
  99. [101]Walter P and Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081– 1086. 22116877
  100. [102]Zhang S, Burkett TJ, Yamashita I and Garfinkel DJ (1997) Genetic redundancy between SPT23 and MGA2: regulators of Ty‐induced mutations and Ty1 transcription in Saccharomyces cerevisiae. Mol Cell Biol 17, 4718– 4729. 9234728 PMC232324
  101. [103]Zhang S, Skalsky Y and Garfinkel DJ (1999) MGA2 or SPT23 is required for transcription of the delta9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 151, 473– 483. 9927444 PMC1460504
  102. [104]Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD and Jentsch S (2000) Activation of a membrane‐bound transcription factor by regulated ubiquitin/proteasome‐dependent processing. Cell 102, 577– 586. 11007476
  103. [105]Covino R, Ballweg S, Stordeur C, Michaelis JB, Puth K, Wernig F, Bahrami A, Ernst AM, Hummer G and Ernst R (2016) A eukaryotic sensor for membrane lipid saturation. Mol Cell 63, 49– 59. 27320200
  104. [106]Surma MA, Klose C, Peng D, Shales M, Mrejen C, Stefanko A, Braberg H, Gordon DE, Vorkel D, Ejsing CS et al (2013) A lipid E‐MAP identifies Ubx2 as a critical regulator of lipid saturation and lipid bilayer stress. Mol Cell 51, 519– 530. 23891562 PMC3791312
  105. [107]Pineau L, Colas J, Dupont S, Beney L, Fleurat‐Lessard P, Berjeaud JM, Berges T and Ferreira T (2009) Lipid‐induced ER stress: synergistic effects of sterols and saturated fatty acids. Traffic 10, 673– 690. 19302420
  106. [108]Halbleib K, Pesek K, Covino R, Hofbauer HF, Wunnicke D, Hanelt I, Hummer G and Ernst R (2017) Activation of the unfolded protein response by lipid bilayer stress. Mol Cell 67, 673– 684. e8 28689662
  107. [109]Schuck S, Prinz WA, Thorn KS, Voss C and Walter P (2009) Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187, 525– 536. 19948500 PMC2779237
  108. [110]Tehlivets O, Scheuringer K and Kohlwein SD (2007) Fatty acid synthesis and elongation in yeast. Biochem Biophys Acta 1771, 255– 270. 16950653
  109. [111]Suzuki K, Akioka M, Kondo‐Kakuta C, Yamamoto H and Ohsumi Y (2013) Fine mapping of autophagy‐related proteins during autophagosome formation in Saccharomyces cerevisiae. J Cell Sci 126, 2534– 2544. 23549786
  110. [112]Graef M, Friedman JR, Graham C, Babu M and Nunnari J (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24, 2918– 2931. 23904270 PMC3771953
  111. [113]Dupont N, Chauhan S, Arko‐Mensah J, Castillo EF, Masedunskas A, Weigert R, Robenek H, Proikas‐Cezanne T and Deretic V (2014) Neutral lipid stores and lipase PNPLA5 contribute to autophagosome biogenesis. Curr Biol 24, 609– 620. 24613307 PMC4016984

Cited by

Sorted by citations

Authors
Graef, M.
Affiliations
University of Cologne (DE)
Corresponding author
Graef, Martin
ORCID
Graef, Martin
Venue
FEBS Letters
Publisher
Wiley
Published
2018-02-16
Volume
592
Issue
8
Pages
1291-1303
ISSN
  • 0014-5793 (ISSN-L)
  • 1873-3468
DOI
10.1002/1873-3468.12996
PMC
PMC5947121
OpenAlex
W2792238812
Cited by
65
References
2
Citations by year
2026: 9 · 2025: 10 · 2024: 6 · 2023: 7 · 2022: 10 · 2021: 5 · 2020: 6 · 2019: 11 · 2018: 1
FWCI
0.56
Type
journal article
Language
en
Open access
Licence
Locations
  • FEBS Letters (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (SFB 1218/TP A04)
  • Max-Planck-Gesellschaft
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords
lipid droplets, lipid homeostasis, proteostasis, lipid metabolism, membrane homeostasis, organelle homeostasis, autophagy, stress tolerance, Saccharomyces cerevisiae
MeSH terms
Homeostasis, Saccharomyces cerevisiae, Saccharomyces cerevisiae Proteins, Lipid Metabolism, Lipid Droplets

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review