1932

Abstract

Lipids are more than biomolecules for energy storage and membrane structure. With ample structural variation, lipids critically participate in nearly all aspects of cellular function. Lipid homeostasis and metabolism are closely related to major human diseases and health problems. However, lipid functional studies have been significantly underdeveloped, partly because of the difficulty in applying genetics and common molecular approaches to tackle the complexity associated with lipid biosynthesis, metabolism, and function. In the past decade, a number of laboratories began to analyze the roles of lipid metabolism in development and other physiological functions using animal models and combining genetics, genomics, and biochemical approaches. These pioneering efforts have not only provided valuable insights regarding lipid functions in vivo but have also established feasible methodology for future studies. Here, we review a subset of these studies using and .

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2014-11-23
2024-04-26
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Literature Cited

  1. Acharya U, Mowen MB, Nagashima K, Acharya JK. 1.  2004. Ceramidase expression facilitates membrane turnover and endocytosis of rhodopsin in photoreceptors. Proc. Natl. Acad. Sci. USA 101:1922–26 [Google Scholar]
  2. Acharya U, Patel S, Koundakjian E, Nagashima K, Han X, Acharya JK. 2.  2003. Modulating sphingolipid biosynthetic pathway rescues photoreceptor degeneration. Science 299:1740–43 [Google Scholar]
  3. Adachi-Yamada T, Gotoh T, Sugimura I, Tateno M, Nishida Y. 3.  et al. 1999. De novo synthesis of sphingolipids is required for cell survival by down-regulating c-Jun N-terminal kinase in Drosophila imaginal discs. Mol. Cell. Biol. 19:7276–86 [Google Scholar]
  4. Arsenault BJ, Boekholdt SM, Kastelein JJ. 4.  2011. Lipid parameters for measuring risk of cardiovascular disease. Nat. Rev. Cardiol. 8:197–206 [Google Scholar]
  5. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS. 5.  et al. 2003. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421:268–72 [Google Scholar]
  6. Atilla-Gokcumen GE, Muro E, Relat-Goberna J, Sasse S, Bedigian A. 6.  et al. 2014. Dividing cells regulate their lipid composition and localization. Cell 156:428–39 [Google Scholar]
  7. Bauer R, Voelzmann A, Breiden B, Schepers U, Farwanah H. 7.  et al. 2009. Schlank, a member of the ceramide synthase family controls growth and body fat in Drosophila. EMBO J. 28:3706–16 [Google Scholar]
  8. Baugh LR, Sternberg PW. 8.  2006. DAF-16/FOXO regulates transcription of cki-1/Cip/Kip and repression of lin-4 during C. elegans L1 arrest. Curr. Biol. 16:780–85 [Google Scholar]
  9. Ben Gedalya T, Loeb V, Israeli E, Altschuler Y, Selkoe DJ, Sharon R. 9.  2009. α-Synuclein and polyunsaturated fatty acids promote clathrin-mediated endocytosis and synaptic vesicle recycling. Traffic 10:218–34 [Google Scholar]
  10. Benton R, Vannice KS, Vosshall LB. 10.  2007. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–93 [Google Scholar]
  11. Brand AH, Perrimon N. 11.  1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–15 [Google Scholar]
  12. Branicky R, Desjardins D, Liu JL, Hekimi S. 12.  2010. Lipid transport and signaling in Caenorhabditis elegans. Dev. Dyn. 239:1365–77 [Google Scholar]
  13. Brendza KM, Haakenson W, Cahoon RE, Hicks LM, Palavalli LH. 13.  et al. 2007. Phosphoethanolamine N-methyltransferase (PMT-1) catalyses the first reaction of a new pathway for phosphocholine biosynthesis in Caenorhabditis elegans. Biochem. J. 404:439–48 [Google Scholar]
  14. Brock TJ, Browse J, Watts JL. 14.  2007. Fatty acid desaturation and the regulation of adiposity in Caenorhabditis elegans. Genetics 176:865–75 [Google Scholar]
  15. Brown MS, Goldstein JL. 15.  1997. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331–40 [Google Scholar]
  16. Carrasco S, Merida I. 16.  2007. Diacylglycerol, when simplicity becomes complex. Trends Biochem. Sci. 32:27–36 [Google Scholar]
  17. Carvalho M, Schwudke D, Sampaio JL, Palm W, Riezman I. 17.  et al. 2010. Survival strategies of a sterol auxotroph. Development 137:3675–85 [Google Scholar]
  18. Chan JP, Hu Z, Sieburth D. 18.  2012. Recruitment of sphingosine kinase to presynaptic terminals by a conserved muscarinic signaling pathway promotes neurotransmitter release. Genes Dev. 26:1070–85 [Google Scholar]
  19. Chen H, Liu Z, Huang X. 19.  2010. Drosophila models of peroxisomal biogenesis disorder: peroxins are required for spermatogenesis and very-long-chain fatty acid metabolism. Hum. Mol. Genet. 19:494–505 [Google Scholar]
  20. Chen Y, Liu Y, Sullards MC, Merrill AH Jr. 20.  2010. An introduction to sphingolipid metabolism and analysis by new technologies. Neuromol. Med. 12:306–19 [Google Scholar]
  21. Chen YZ, Mapes J, Lee ES, Skeen-Gaar RR, Xue D. 21.  2013. Caspase-mediated activation of Caenorhabditis elegans CED-8 promotes apoptosis and phosphatidylserine externalization. Nat. Commun. 4:2726 [Google Scholar]
  22. Chertemps T, Duportets L, Labeur C, Ueda R, Takahashi K. 22.  et al. 2007. A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104:4273–78 [Google Scholar]
  23. Chertemps T, Duportets L, Labeur C, Ueyama M, Wicker-Thomas C. 23.  2006. A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol. Biol. 15:465–73 [Google Scholar]
  24. Chitwood DJ, Lusby WR, Thompson MJ, Kochansky JP, Howarth OW. 24.  1995. The glycosylceramides of the nematode Caenorhabditis elegans contain an unusual, branched-chain sphingoid base. Lipids 30:567–73 [Google Scholar]
  25. Coetzee T, Fujita N, Dupree J, Shi R, Blight A. 25.  et al. 1996. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 86:209–19 [Google Scholar]
  26. Dallerac R, Labeur C, Jallon JM, Knipple DC, Roelofs WL, Wicker-Thomas C. 26.  2000. A Δ9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 97:9449–54 [Google Scholar]
  27. Darland-Ransom M, Wang X, Sun CL, Mapes J, Gengyo-Ando K. 27.  et al. 2008. Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320:528–31 [Google Scholar]
  28. Dasgupta U, Bamba T, Chiantia S, Karim P, Tayoun AN. 28.  et al. 2009. Ceramide kinase regulates phospholipase C and phosphatidylinositol 4, 5, bisphosphate in phototransduction. Proc. Natl. Acad. Sci. USA 106:20063–68 [Google Scholar]
  29. Deng X, Yin X, Allan R, Lu DD, Maurer CW. 29.  et al. 2008. Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans. Science 322:110–15 [Google Scholar]
  30. Di Marzo V, Bifulco M, De Petrocellis L. 30.  2004. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3:771–84 [Google Scholar]
  31. Dobrosotskaya IY, Seegmiller AC, Brown MS, Goldstein JL, Rawson RB. 31.  2002. Regulation of SREBP processing and membrane lipid production by phospholipids in Drosophila. Science 296:879–83 [Google Scholar]
  32. Edmonds JW, Prasain JK, Dorand D, Yang Y, Hoang HD. 32.  et al. 2010. Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev. Cell 19:858–71 [Google Scholar]
  33. Ejima A, Smith BP, Lucas C, van der Goes van Naters W, Miller CJ. 33.  et al. 2007. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17:599–605 [Google Scholar]
  34. Engelman JA, Luo J, Cantley LC. 34.  2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7:606–19 [Google Scholar]
  35. Entchev EV, Schwudke D, Zagoriy V, Matyash V, Bogdanova A. 35.  et al. 2008. LET-767 is required for the production of branched chain and long chain fatty acids in Caenorhabditis elegans. J. Biol. Chem. 283:17550–60 [Google Scholar]
  36. Ewers H, Helenius A. 36.  2011. Lipid-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 3:a004721 [Google Scholar]
  37. Fabian L, Wei HC, Rollins J, Noguchi T, Blankenship JT. 37.  et al. 2010. Phosphatidylinositol 4,5-bisphosphate directs spermatid cell polarity and exocyst localization in Drosophila. Mol. Biol. Cell 21:1546–55 [Google Scholar]
  38. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. 38.  1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207–16 [Google Scholar]
  39. Fagone P, Jackowski S. 39.  2009. Membrane phospholipid synthesis and endoplasmic reticulum function. J. Lipid Res. 50:Suppl.S311–16 [Google Scholar]
  40. Ferveur JF. 40.  2005. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35:279–95 [Google Scholar]
  41. Friesen JA, Liu MF, Kent C. 41.  2001. Cloning and characterization of a lipid-activated CTP:phosphocholine cytidylyltransferase from Caenorhabditis elegans: identification of a 21-residue segment critical for lipid activation. Biochim. Biophys. Acta153386–98
  42. Fuchs B, Suss R, Teuber K, Eibisch M, Schiller J. 42.  2011. Lipid analysis by thin-layer chromatography: a review of the current state. J. Chromatogr. A 1218:2754–74 [Google Scholar]
  43. Fyrst H, Saba JD. 43.  2010. An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat. Chem. Biol. 6:489–97 [Google Scholar]
  44. Gallet A, Rodriguez R, Ruel L, Therond PP. 44.  2003. Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetric cellular response to hedgehog. Dev. Cell 4:191–204 [Google Scholar]
  45. Gault CR, Obeid LM, Hannun YA. 45.  2010. An overview of sphingolipid metabolism: from synthesis to breakdown. Adv. Exp. Med. Biol. 688:1–23 [Google Scholar]
  46. Golomb BA, Evans MA. 46.  2008. Statin adverse effects: a review of the literature and evidence for a mitochondrial mechanism. Am. J. Cardiovasc. Drugs 8:373–418 [Google Scholar]
  47. Gomez-Diaz C, Reina JH, Cambillau C, Benton R. 47.  2013. Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins. PLOS Biol. 11:e1001546 [Google Scholar]
  48. Goode S, Melnick M, Chou TB, Perrimon N. 48.  1996. The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis. Development 122:3863–79 [Google Scholar]
  49. Griffiths WJ, Wang Y. 49.  2009. Mass spectrometry: from proteomics to metabolomics and lipidomics. Chem. Soc. Rev. 38:1882–96 [Google Scholar]
  50. Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B. 50.  et al. 2005. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307:922–25 [Google Scholar]
  51. Griffitts JS, Whitacre JL, Stevens DE, Aroian RV. 51.  2001. Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293:860–64 [Google Scholar]
  52. Groen CM, Spracklen AJ, Fagan TN, Tootle TL. 52.  2012. Drosophila Fascin is a novel downstream target of prostaglandin signaling during actin remodeling. Mol. Biol. Cell 23:4567–78 [Google Scholar]
  53. Gronke S, Mildner A, Fellert S, Tennagels N, Petry S. 53.  et al. 2005. Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1:323–30 [Google Scholar]
  54. Guan XL, Cestra G, Shui G, Kuhrs A, Schittenhelm RB. 54.  et al. 2013. Biochemical membrane lipidomics during Drosophila development. Dev. Cell 24:98–111 [Google Scholar]
  55. Guillou H, Zadravec D, Martin PG, Jacobsson A. 55.  2010. The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog. Lipid Res. 49:186–99 [Google Scholar]
  56. Gupta GD, Swetha MG, Kumari S, Lakshminarayan R, Dey G, Mayor S. 56.  2009. Analysis of endocytic pathways in Drosophila cells reveals a conserved role for GBF1 in internalization via GEECs. PLOS ONE 4:e6768 [Google Scholar]
  57. Gupta T, Schupbach T. 57.  2003. Cct1, a phosphatidylcholine biosynthesis enzyme, is required for Drosophila oogenesis and ovarian morphogenesis. Development 130:6075–87 [Google Scholar]
  58. Hakomori S. 58.  2000. Traveling for the glycosphingolipid path. Glycoconj. J. 17:627–47 [Google Scholar]
  59. Hamel S, Fantini J, Schweisguth F. 59.  2010. Notch ligand activity is modulated by glycosphingolipid membrane composition in Drosophila melanogaster. J. Cell Biol. 188:581–94 [Google Scholar]
  60. Hammad LA, Cooper BS, Fisher NP, Montooth KL, Karty JA. 60.  2011. Profiling and quantification of Drosophila melanogaster lipids using liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 25:2959–68 [Google Scholar]
  61. Han X, Gross RW. 61.  2005. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24:367–412 [Google Scholar]
  62. Hannich JT, Entchev EV, Mende F, Boytchev H, Martin R. 62.  et al. 2009. Methylation of the sterol nucleus by STRM-1 regulates dauer larva formation in Caenorhabditis elegans. Dev. Cell 16:833–43 [Google Scholar]
  63. Hansen M, Flatt T, Aguilaniu H. 63.  2013. Reproduction, fat metabolism, and life span: What is the connection?. Cell Metab. 17:10–19 [Google Scholar]
  64. Harris WS, Mozaffarian D, Lefevre M, Toner CD, Colombo J. 64.  et al. 2009. Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J. Nutr. 139:804S–19 [Google Scholar]
  65. Hebbar S, Lee E, Manna M, Steinert S, Kumar GS. 65.  et al. 2008. A fluorescent sphingolipid binding domain peptide probe interacts with sphingolipids and cholesterol-dependent raft domains. J. Lipid Res. 49:1077–89 [Google Scholar]
  66. Herr DR, Fyrst H, Creason MB, Phan VH, Saba JD, Harris GL. 66.  2004. Characterization of the Drosophila sphingosine kinases and requirement for Sk2 in normal reproductive function. J. Biol. Chem. 279:12685–94 [Google Scholar]
  67. Herr DR, Fyrst H, Phan V, Heinecke K, Georges R. 67.  et al. 2003. Sply regulation of sphingolipid signaling molecules is essential for Drosophila development. Development 130:2443–53 [Google Scholar]
  68. Hla T, Dannenberg AJ. 68.  2012. Sphingolipid signaling in metabolic disorders. Cell Metab. 16:420–34 [Google Scholar]
  69. Hoang HD, Prasain JK, Dorand D, Miller MA. 69.  2013. A heterogeneous mixture of F-series prostaglandins promotes sperm guidance in the Caenorhabditis elegans reproductive tract. PLOS Genet. 9:e1003271 [Google Scholar]
  70. Hoeferlin LA, Wijesinghe DS, Chalfant CE. 70.  2013. The role of ceramide-1-phosphate in biological functions. Handb. Exp. Pharmacol. 215:153–66 [Google Scholar]
  71. Horikawa M, Nomura T, Hashimoto T, Sakamoto K. 71.  2008. Elongation and desaturation of fatty acids are critical in growth, lipid metabolism and ontogeny of Caenorhabditis elegans. J. Biochem. 144:149–58 [Google Scholar]
  72. Horner MA, Pardee K, Liu S, King-Jones K, Lajoie G. 72.  et al. 2009. The Drosophila DHR96 nuclear receptor binds cholesterol and regulates cholesterol homeostasis. Genes Dev. 23:2711–16 [Google Scholar]
  73. Huang X, Warren JT, Buchanan J, Gilbert LI, Scott MP. 73.  2007. Drosophila Niemann-Pick Type C-2 genes control sterol homeostasis and steroid biosynthesis: a model of human neurodegenerative disease. Development 134:3733–42 [Google Scholar]
  74. Huber TB, Schermer B, Muller RU, Hohne M, Bartram M. 74.  et al. 2006. Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc. Natl. Acad. Sci. USA 103:17079–86 [Google Scholar]
  75. Imae R, Inoue T, Kimura M, Kanamori T, Tomioka NH. 75.  et al. 2010. Intracellular phospholipase A1 and acyltransferase, which are involved in Caenorhabditis elegans stem cell divisions, determine the sn-1 fatty acyl chain of phosphatidylinositol. Mol. Biol. Cell 21:3114–24 [Google Scholar]
  76. Iwata R, Oda S, Kunitomo H, Iino Y. 76.  2011. Roles for class IIA phosphatidylinositol transfer protein in neurotransmission and behavioral plasticity at the sensory neuron synapses of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 108:7589–94 [Google Scholar]
  77. Jakobsson A, Westerberg R, Jacobsson A. 77.  2006. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45:237–49 [Google Scholar]
  78. Jones LN, Rivett DE. 78.  1997. The role of 18-methyleicosanoic acid in the structure and formation of mammalian hair fibres. Micron 28:469–85 [Google Scholar]
  79. Kadamur G, Ross EM. 79.  2013. Mammalian phospholipase C. Annu. Rev. Physiol. 75:127–54 [Google Scholar]
  80. Kage-Nakadai E, Kobuna H, Kimura M, Gengyo-Ando K, Inoue T. 80.  et al. 2010. Two very long chain fatty acid acyl-CoA synthetase genes, acs-20 and acs-22, have roles in the cuticle surface barrier in Caenorhabditis elegans. PLOS ONE 5:e8857 [Google Scholar]
  81. Kahn-Kirby AH, Dantzker JL, Apicella AJ, Schafer WR, Browse J. 81.  et al. 2004. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119:889–900 [Google Scholar]
  82. Kaneda T, Smith EJ. 82.  1980. Relationship of primer specificity of fatty acid de novo synthetase to fatty acid composition in 10 species of bacteria and yeasts. Can. J. Microbiol. 26:893–98 [Google Scholar]
  83. Katic I, Vallier LG, Greenwald I. 83.  2005. New positive regulators of lin-12 activity in Caenorhabditis elegans include the BRE-5/Brainiac glycosphingolipid biosynthesis enzyme. Genetics 171:1605–15 [Google Scholar]
  84. Keleman K, Vrontou E, Kruttner S, Yu JY, Kurtovic-Kozaric A, Dickson BJ. 84.  2012. Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489:145–49 [Google Scholar]
  85. Kho Y, Kim SC, Jiang C, Barma D, Kwon SW. 85.  et al. 2004. A tagging-via-substrate technology for detection and proteomics of farnesylated proteins. Proc. Natl. Acad. Sci. USA 101:12479–84 [Google Scholar]
  86. Khuong TM, Habets RL, Slabbaert JR, Verstreken P. 86.  2010. WASP is activated by phosphatidylinositol-4,5-bisphosphate to restrict synapse growth in a pathway parallel to bone morphogenetic protein signaling. Proc. Natl. Acad. Sci. USA 107:17379–84 [Google Scholar]
  87. Klopfenstein DR, Tomishige M, Stuurman N, Vale RD. 87.  2002. Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109:347–58 [Google Scholar]
  88. Kniazeva M, Crawford QT, Seiber M, Wang CY, Han M. 88.  2004. Monomethyl branched-chain fatty acids play an essential role in Caenorhabditis elegans development. PLOS Biol. 2:E257 [Google Scholar]
  89. Kniazeva M, Euler T, Han M. 89.  2008. A branched-chain fatty acid is involved in post-embryonic growth control in parallel to the insulin receptor pathway and its biosynthesis is feedback-regulated in C. elegans. Genes Dev. 22:2102–10 [Google Scholar]
  90. Kniazeva M, Shen H, Euler T, Wang C, Han M. 90.  2012. Regulation of maternal phospholipid composition and IP3-dependent embryonic membrane dynamics by a specific fatty acid metabolic event in C. elegans. Genes Dev. 26:554–66 [Google Scholar]
  91. Kniazeva M, Sieber M, McCauley S, Zhang K, Watts JL, Han M. 91.  2003. Suppression of the ELO-2 FA elongation activity results in alterations of the fatty acid composition and multiple physiological defects, including abnormal ultradian rhythms, in Caenorhabditis elegans. Genetics 163:159–69 [Google Scholar]
  92. Kohyama-Koganeya A, Nabetani T, Miura M, Hirabayashi Y. 92.  2011. Glucosylceramide synthase in the fat body controls energy metabolism in Drosophila. J. Lipid Res. 52:1392–99 [Google Scholar]
  93. Krahmer N, Guo Y, Wilfling F, Hilger M, Lingrell S. 93.  et al. 2011. Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab. 14:504–15 [Google Scholar]
  94. Krieser RJ, Moore FE, Dresnek D, Pellock BJ, Patel R. 94.  et al. 2007. The Drosophila homolog of the putative phosphatidylserine receptor functions to inhibit apoptosis. Development 134:2407–14 [Google Scholar]
  95. Kubagawa HM, Watts JL, Corrigan C, Edmonds JW, Sztul E. 95.  et al. 2006. Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat. Cell Biol. 8:1143–48 [Google Scholar]
  96. Kuhnlein RP. 96.  2011. The contribution of the Drosophila model to lipid droplet research. Prog. Lipid Res. 50:348–56 [Google Scholar]
  97. Kurtovic A, Widmer A, Dickson BJ. 97.  2007. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–46 [Google Scholar]
  98. Kurzchalia TV, Ward S. 98.  2003. Why do worms need cholesterol?. Nat. Cell Biol. 5:684–88 [Google Scholar]
  99. Lagace TA, Ridgway ND. 99.  2013. The role of phospholipids in the biological activity and structure of the endoplasmic reticulum. Biochim. Biophys. Acta 1833:2499–510 [Google Scholar]
  100. Laughlin JD, Ha TS, Jones DN, Smith DP. 100.  2008. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133:1255–65 [Google Scholar]
  101. Lee BH, Ashrafi K. 101.  2008. A TRPV channel modulates C. elegans neurosecretion, larval starvation survival, and adult lifespan. PLOS Genet. 4:e1000213 [Google Scholar]
  102. Lee HC, Inoue T, Imae R, Kono N, Shirae S. 102.  et al. 2008. Caenorhabditis elegans mboa-7, a member of the MBOAT family, is required for selective incorporation of polyunsaturated fatty acids into phosphatidylinositol. Mol. Biol. Cell 19:1174–84 [Google Scholar]
  103. Lehtonen M, Reisner K, Auriola S, Wong G, Callaway JC. 103.  2008. Mass-spectrometric identification of anandamide and 2-arachidonoylglycerol in nematodes. Chem. Biodivers. 5:2431–41 [Google Scholar]
  104. Leibundgut M, Maier T, Jenni S, Ban N. 104.  2008. The multienzyme architecture of eukaryotic fatty acid synthases. Curr. Opin. Struct. Biol. 18:714–25 [Google Scholar]
  105. Lesa GM, Palfreyman M, Hall DH, Clandinin MT, Rudolph C. 105.  et al. 2003. Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans. J. Cell Sci. 116:4965–75 [Google Scholar]
  106. Li Y, Zhang H, Litingtung Y, Chiang C. 106.  2006. Cholesterol modification restricts the spread of Shh gradient in the limb bud. Proc. Natl. Acad. Sci. USA 103:6548–53 [Google Scholar]
  107. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R. 107.  et al. 1997. Multiple female reproductive failures in cyclooxygenase 2–deficient mice. Cell 91:197–208 [Google Scholar]
  108. Lim HY, Wang W, Wessells RJ, Ocorr K, Bodmer R. 108.  2011. Phospholipid homeostasis regulates lipid metabolism and cardiac function through SREBP signaling in Drosophila. Genes Dev. 25:189–200 [Google Scholar]
  109. Lingwood D, Simons K. 109.  2010. Lipid rafts as a membrane-organizing principle. Science 327:46–50 [Google Scholar]
  110. Liu JL, Desjardins D, Branicky R, Agellon LB, Hekimi S. 110.  2012. Mitochondrial oxidative stress alters a pathway in Caenorhabditis elegans strongly resembling that of bile acid biosynthesis and secretion in vertebrates. PLOS Genet. 8:e1002553 [Google Scholar]
  111. Liu W, Liang X, Gong J, Yang Z, Zhang YH. 111.  et al. 2011. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat. Neurosci. 14:896–902 [Google Scholar]
  112. Lu N, Shen Q, Mahoney TR, Neukomm LJ, Wang Y, Zhou Z. 112.  2012. Two PI 3-kinases and one PI 3-phosphatase together establish the cyclic waves of phagosomal PtdIns(3)P critical for the degradation of apoptotic cells. PLOS Biol. 10:e1001245 [Google Scholar]
  113. Lucanic M, Held JM, Vantipalli MC, Klang IM, Graham JB. 113.  et al. 2011. N-acylethanolamine signalling mediates the effect of diet on lifespan in Caenorhabditis elegans. Nature 473:226–29 [Google Scholar]
  114. Ma DK, Rothe M, Zheng S, Bhatla N, Pender CL. 114.  et al. 2013. Cytochrome P450 drives a HIF-regulated behavioral response to reoxygenation by C. elegans. Science 341:554–58 [Google Scholar]
  115. Malhotra A, Xu Y, Ren M, Schlame M. 115.  2009. Formation of molecular species of mitochondrial cardiolipin. 1. A novel transacylation mechanism to shuttle fatty acids between sn-1 and sn-2 positions of multiple phospholipid species. Biochim. Biophys. Acta 1791:314–20 [Google Scholar]
  116. Marek LR, Kagan JC. 116.  2012. Phosphoinositide binding by the Toll adaptor dMyD88 controls antibacterial responses in Drosophila. Immunity 36:612–22 [Google Scholar]
  117. Marza E, Long T, Saiardi A, Sumakovic M, Eimer S. 117.  et al. 2008. Polyunsaturated fatty acids influence synaptojanin localization to regulate synaptic vesicle recycling. Mol. Biol. Cell 19:833–42 [Google Scholar]
  118. Marza E, Simonsen KT, Faergeman NJ, Lesa GM. 118.  2009. Expression of ceramide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells. J. Cell Sci. 122:822–33 [Google Scholar]
  119. Matyash V, Geier C, Henske A, Mukherjee S, Hirsh D. 119.  et al. 2001. Distribution and transport of cholesterol in Caenorhabditis elegans. Mol. Biol. Cell 12:1725–36 [Google Scholar]
  120. Maxfield FR, Tabas I. 120.  2005. Role of cholesterol and lipid organization in disease. Nature 438:612–21 [Google Scholar]
  121. Mayinger P. 121.  2012. Phosphoinositides and vesicular membrane traffic. Biochim. Biophys. Acta 1821:1104–13 [Google Scholar]
  122. McMahon A, Butovich IA, Kedzierski W. 122.  2011. Epidermal expression of an Elovl4 transgene rescues neonatal lethality of homozygous Stargardt disease-3 mice. J. Lipid Res. 52:1128–38 [Google Scholar]
  123. McPhee CK, Logan MA, Freeman MR, Baehrecke EH. 123.  2010. Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 465:1093–96 [Google Scholar]
  124. Meloni I, Muscettola M, Raynaud M, Longo I, Bruttini M. 124.  et al. 2002. FACL4, encoding fatty acid-CoA ligase 4, is mutated in nonspecific X-linked mental retardation. Nat. Genet. 30:436–40 [Google Scholar]
  125. Mendel J, Heinecke K, Fyrst H, Saba JD. 125.  2003. Sphingosine phosphate lyase expression is essential for normal development in Caenorhabditis elegans. J. Biol. Chem. 278:22341–49 [Google Scholar]
  126. Menuz V, Howell KS, Gentina S, Epstein S, Riezman I. 126.  et al. 2009. Protection of C. elegans from anoxia by HYL-2 ceramide synthase. Science 324:381–84 [Google Scholar]
  127. Merrill AH Jr, Schmelz EM, Dillehay DL, Spiegel S, Shayman JA. 127.  et al. 1997. Sphingolipids—the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol. Appl. Pharmacol. 142:208–25 [Google Scholar]
  128. Morck C, Olsen L, Kurth C, Persson A, Storm NJ. 128.  et al. 2009. Statins inhibit protein lipidation and induce the unfolded protein response in the non-sterol producing nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 106:18285–90 [Google Scholar]
  129. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T. 129.  et al. 2006. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124:1209–23 [Google Scholar]
  130. Mullen TD, Hannun YA, Obeid LM. 130.  2012. Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem. J. 441:789–802 [Google Scholar]
  131. Nandakumar M, Tan MW. 131.  2008. Gamma-linolenic and stearidonic acids are required for basal immunity in Caenorhabditis elegans through their effects on p38 MAP kinase activity. PLOS Genet. 4:e1000273 [Google Scholar]
  132. Nezis IP, Sagona AP, Schink KO, Stenmark H. 132.  2010. Divide and ProsPer: the emerging role of PtdIns3P in cytokinesis. Trends Cell Biol. 20:642–49 [Google Scholar]
  133. O'Rourke EJ, Kuballa P, Xavier R, Ruvkun G. 133.  2013. Omega-6 polyunsaturated fatty acids extend life span through the activation of autophagy. Genes Dev. 27:429–40 [Google Scholar]
  134. Pagano RE, Martin OC, Kang HC, Haugland RP. 134.  1991. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113:1267–79 [Google Scholar]
  135. Palavalli LH, Brendza KM, Haakenson W, Cahoon RE, McLaird M. 135.  et al. 2006. Defining the role of phosphomethylethanolamine N-methyltransferase from Caenorhabditis elegans in phosphocholine biosynthesis by biochemical and kinetic analysis. Biochemistry 45:6056–65 [Google Scholar]
  136. Panbianco C, Weinkove D, Zanin E, Jones D, Divecha N. 136.  et al. 2008. A casein kinase 1 and PAR proteins regulate asymmetry of a PIP(2) synthesis enzyme for asymmetric spindle positioning. Dev. Cell 15:198–208 [Google Scholar]
  137. Pantoja M, Fischer KA, Ieronimakis N, Reyes M, Ruohola-Baker H. 137.  2013. Genetic elevation of sphingosine 1–phosphate suppresses dystrophic muscle phenotypes in Drosophila. Development 140:136–46 [Google Scholar]
  138. Parvy JP, Napal L, Rubin T, Poidevin M, Perrin L. 138.  et al. 2012. Drosophila melanogaster acetyl-CoA-carboxylase sustains a fatty acid–dependent remote signal to waterproof the respiratory system. PLOS Genet. 8:e1002925 [Google Scholar]
  139. Pastuhov SI, Fujiki K, Nix P, Kanao S, Bastiani M. 139.  et al. 2012. Endocannabinoid-Goα signalling inhibits axon regeneration in Caenorhabditis elegans by antagonizing Gqα-PKC-JNK signalling. Nat. Commun. 3:1136 [Google Scholar]
  140. Patel DS, Fang LL, Svy DK, Ruvkun G, Li W. 140.  2008. Genetic identification of HSD-1, a conserved steroidogenic enzyme that directs larval development in Caenorhabditis elegans. Development 135:2239–49 [Google Scholar]
  141. Paulick MG, Bertozzi CR. 141.  2008. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47:6991–7000 [Google Scholar]
  142. Piomelli D. 142.  2003. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4:873–84 [Google Scholar]
  143. Pizette S, Rabouille C, Cohen SM, Therond P. 143.  2009. Glycosphingolipids control the extracellular gradient of the Drosophila EGFR ligand Gurken. Development 136:551–61 [Google Scholar]
  144. Poccia D, Larijani B. 144.  2009. Phosphatidylinositol metabolism and membrane fusion. Biochem. J. 418:233–46 [Google Scholar]
  145. Poulos A. 145.  1995. Very long chain fatty acids in higher animals: a review. Lipids 30:1–14 [Google Scholar]
  146. Ran-Ressler RR, Sim D, O'Donnell-Megaro AM, Bauman DE, Barbano DM, Brenna JT. 146.  2011. Branched chain fatty acid content of United States retail cow's milk and implications for dietary intake. Lipids 46:569–76 [Google Scholar]
  147. Rasmussen JA, Hermetter A. 147.  2008. Chemical synthesis of fluorescent glycero- and sphingolipids. Prog. Lipid Res. 47:436–60 [Google Scholar]
  148. Rauthan M, Pilon M. 148.  2011. The mevalonate pathway in C. elegans. Lipids Health Dis. 10:243 [Google Scholar]
  149. Rauthan M, Ranji P, Aguilera Pradenas N, Pitot C, Pilon M. 149.  2013. The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proc. Natl. Acad. Sci. USA 110:5981–86 [Google Scholar]
  150. Ribeiro I, Yuan L, Tanentzapf G, Dowling JJ, Kiger A. 150.  2011. Phosphoinositide regulation of integrin trafficking required for muscle attachment and maintenance. PLOS Genet. 7:e1001295 [Google Scholar]
  151. Roncaglioni MC, Tombesi M, Avanzini F, Barlera S, Caimi V. 151.  et al. 2013. n-3 fatty acids in patients with multiple cardiovascular risk factors. N. Engl. J. Med. 368:1800–8 [Google Scholar]
  152. Roth GE, Gierl MS, Vollborn L, Meise M, Lintermann R, Korge G. 152.  2004. The Drosophila gene Start1: a putative cholesterol transporter and key regulator of ecdysteroid synthesis. Proc. Natl. Acad. Sci. USA 101:1601–6 [Google Scholar]
  153. Sabourdy F, Kedjouar B, Sorli SC, Colie S, Milhas D. 153.  et al. 2008. Functions of sphingolipid metabolism in mammals: lessons from genetic defects. Biochim. Biophys. Acta 1781:145–83 [Google Scholar]
  154. Santos AC, Lehmann R. 154.  2004. Isoprenoids control germ cell migration downstream of HMGCoA reductase. Dev. Cell 6:283–93 [Google Scholar]
  155. Sasamura T, Matsuno K, Fortini ME. 155.  2013. Disruption of Drosophila melanogaster lipid metabolism genes causes tissue overgrowth associated with altered developmental signaling. PLOS Genet. 9:e1003917 [Google Scholar]
  156. Satoh T, Inagaki T, Liu Z, Watanabe R, Satoh AK. 156.  2013. GPI biosynthesis is essential for rhodopsin sorting at the trans-Golgi network in Drosophila photoreceptors. Development 140:385–94 [Google Scholar]
  157. Schwientek T, Keck B, Levery SB, Jensen MA, Pedersen JW. 157.  et al. 2002. The Drosophila gene brainiac encodes a glycosyltransferase putatively involved in glycosphingolipid synthesis. J. Biol. Chem. 277:32421–29 [Google Scholar]
  158. Scott JL, Musselman CA, Adu-Gyamfi E, Kutateladze TG, Stahelin RV. 158.  2012. Emerging methodologies to investigate lipid-protein interactions. Integr. Biol. 4:247–58 [Google Scholar]
  159. Seamen E, Blanchette JM, Han M. 159.  2009. P-type ATPase TAT-2 negatively regulates monomethyl branched-chain fatty acid mediated function in post-embryonic growth and development in C. elegans. PLOS Genet. 5:e1000589 [Google Scholar]
  160. Seppo A, Moreland M, Schweingruber H, Tiemeyer M. 160.  2000. Zwitterionic and acidic glycosphingolipids of the Drosophila melanogaster embryo. Eur. J. Biochem. 267:3549–58 [Google Scholar]
  161. Shen LR, Lai CQ, Feng X, Parnell LD, Wan JB. 161.  et al. 2010. Drosophila lacks C20 and C22 PUFAs. J. Lipid Res. 51:2985–92 [Google Scholar]
  162. Shim YH, Chun JH, Lee EY, Paik YK. 162.  2002. Role of cholesterol in germ-line development of Caenorhabditis elegans. Mol. Reprod. Dev. 61:358–66 [Google Scholar]
  163. Shindou H, Hishikawa D, Harayama T, Yuki K, Shimizu T. 163.  2009. Recent progress on acyl CoA:lysophospholipid acyltransferase research. J. Lipid Res. 50:Suppl.S46–51 [Google Scholar]
  164. Shindou H, Shimizu T. 164.  2009. Acyl-CoA:lysophospholipid acyltransferases. J. Biol. Chem. 284:1–5 [Google Scholar]
  165. Silhankova M, Port F, Harterink M, Basler K, Korswagen HC. 165.  2010. Wnt signalling requires MTM-6 and MTM-9 myotubularin lipid-phosphatase function in Wnt-producing cells. EMBO J. 29:4094–105 [Google Scholar]
  166. Smith WL. 166.  1989. The eicosanoids and their biochemical mechanisms of action. Biochem. J. 259:315–24 [Google Scholar]
  167. Soupene E, Kuypers FA. 167.  2008. Mammalian long-chain acyl-CoA synthetases. Exp. Biol. Med. (Maywood) 233:507–21 [Google Scholar]
  168. Steinhauer J, Gijon MA, Riekhof WR, Voelker DR, Murphy RC, Treisman JE. 168.  2009. Drosophila lysophospholipid acyltransferases are specifically required for germ cell development. Mol. Biol. Cell 20:5224–35 [Google Scholar]
  169. Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S. 169.  2013. Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 341:403–6 [Google Scholar]
  170. Szafer-Glusman E, Giansanti MG, Nishihama R, Bolival B, Pringle J. 170.  et al. 2008. A role for very-long-chain fatty acids in furrow ingression during cytokinesis in Drosophila spermatocytes. Curr. Biol. 18:1426–31 [Google Scholar]
  171. Tanaka T, Ikita K, Ashida T, Motoyama Y, Yamaguchi Y, Satouchi K. 171.  1996. Effects of growth temperature on the fatty acid composition of the free-living nematode Caenorhabditis elegans. Lipids 31:1173–78 [Google Scholar]
  172. Tanizawa Y, Kuhara A, Inada H, Kodama E, Mizuno T, Mori I. 172.  2006. Inositol monophosphatase regulates localization of synaptic components and behavior in the mature nervous system of C. elegans. Genes Dev. 20:3296–310 [Google Scholar]
  173. Tilley DM, Evans CR, Larson TM, Edwards KA, Friesen JA. 173.  2008. Identification and characterization of the nuclear isoform of Drosophila melanogaster CTP:phosphocholine cytidylyltransferase. Biochemistry 47:11838–46 [Google Scholar]
  174. Tootle TL, Spradling AC. 174.  2008. Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 135:839–47 [Google Scholar]
  175. Vance DE. 175.  2013. Physiological roles of phosphatidylethanolamine N-methyltransferase. Biochim. Biophys. Acta 1831:626–32 [Google Scholar]
  176. Vance JE. 176.  2008. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J. Lipid Res. 49:1377–87 [Google Scholar]
  177. Vance JE, Tasseva G. 177.  2013. Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Biochim. Biophys. Acta 1831:543–54 [Google Scholar]
  178. Vasireddy V, Uchida Y, Salem N Jr., Kim SY, Mandal MN. 178.  et al. 2007. Loss of functional ELOVL4 depletes very long-chain fatty acids (> or = C28) and the unique omega-O-acylceramides in skin leading to neonatal death. Hum. Mol. Genet. 16:471–82 [Google Scholar]
  179. Vasireddy V, Wong P, Ayyagari R. 179.  2010. Genetics and molecular pathology of Stargardt-like macular degeneration. Prog. Retin. Eye Res. 29:191–207 [Google Scholar]
  180. Vrablik TL, Watts JL. 180.  2013. Polyunsaturated fatty acid derived signaling in reproduction and development: insights from Caenorhabditis elegans and Drosophila melanogaster. Mol. Reprod. Dev. 80:244–59 [Google Scholar]
  181. Walker AK, Jacobs RL, Watts JL, Rottiers V, Jiang K. 181.  et al. 2011. A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell 147:840–52 [Google Scholar]
  182. Walther TC, Farese RV Jr. 182.  2012. Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81:687–714 [Google Scholar]
  183. Wandall HH, Pizette S, Pedersen JW, Eichert H, Levery SB. 183.  et al. 2005. Egghead and brainiac are essential for glycosphingolipid biosynthesis in vivo. J. Biol. Chem. 280:4858–63 [Google Scholar]
  184. Wang R, Kniazeva M, Han M. 184.  2013. Peroxisome protein transportation affects metabolism of branched-chain fatty acids that critically impact growth and development of C. elegans. PLOS ONE 8:e76270 [Google Scholar]
  185. Wang X, Wu YC, Fadok VA, Lee MC, Gengyo-Ando K. 185.  et al. 2003. Cell corpse engulfment mediated by C. elegans phosphatidylserine receptor through CED-5 and CED-12. Science 302:1563–66 [Google Scholar]
  186. Watts JL, Browse J. 186.  2002. Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99:5854–59 [Google Scholar]
  187. Watts JL, Browse J. 187.  2006. Dietary manipulation implicates lipid signaling in the regulation of germ cell maintenance in C. elegans. Dev. Biol. 292:381–92 [Google Scholar]
  188. Weber U, Eroglu C, Mlodzik M. 188.  2003. Phospholipid membrane composition affects EGF receptor and Notch signaling through effects on endocytosis during Drosophila development. Dev. Cell 5:559–70 [Google Scholar]
  189. Webster CM, Deline ML, Watts JL. 189.  2013. Stress response pathways protect germ cells from omega-6 polyunsaturated fatty acid–mediated toxicity in Caenorhabditis elegans. Dev. Biol 373:14–25 [Google Scholar]
  190. Wehman AM, Poggioli C, Schweinsberg P, Grant BD, Nance J. 190.  2011. The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr. Biol. 21:1951–59 [Google Scholar]
  191. Wollam J, Magner DB, Magomedova L, Rass E, Shen Y. 191.  et al. 2012. A novel 3-hydroxysteroid dehydrogenase that regulates reproductive development and longevity. PLOS Biol. 10:e1001305 [Google Scholar]
  192. Xu T, Rubin GM. 192.  1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117:1223–37 [Google Scholar]
  193. Yavari A, Nagaraj R, Owusu-Ansah E, Folick A, Ngo K. 193.  et al. 2010. Role of lipid metabolism in smoothened derepression in hedgehog signaling. Dev. Cell 19:54–65 [Google Scholar]
  194. Zhang H, Abraham N, Khan LA, Hall DH, Fleming JT, Gobel V. 194.  2011. Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell Biol. 13:1189–201 [Google Scholar]
  195. Zhang H, Kim A, Abraham N, Khan LA, Hall DH. 195.  et al. 2012. Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 139:2071–83 [Google Scholar]
  196. Zhang K, Kniazeva M, Han M, Li W, Yu Z. 196.  et al. 2001. A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat. Genet. 27:89–93 [Google Scholar]
  197. Zhu H, Shen H, Sewell AK, Kniazeva M, Han M. 197.  2013. A novel sphingolipid-TORC1 pathway critically promotes postembryonic development in Caenorhabditis elegans. Elife 2:e00429 [Google Scholar]
  198. Zullig S, Neukomm LJ, Jovanovic M, Charette SJ, Lyssenko NN. 198.  et al. 2007. Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr. Biol. 17:994–99 [Google Scholar]
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