The life of lipid droplets

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 6, 2009, Pages 459-466

  Walther, Tobias C ^a   Farese Jr , Robert V ^b,c,d  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adiposome; Fat storage; Organelle dynamic; Steryl ester; Triglyceride

Indexed keywords

ADIPOPHILIN; BIOFUEL; FAT DROPLET; LIPID; OIL; PERILIPIN; PROTEIN; TIP47 PROTEIN; UNCLASSIFIED DRUG;

BIOGENESIS; CELL FUSION; CELL INTERACTION; CELL MEMBRANE; CELL MIGRATION; CELL MOTION; CELL ORGANELLE; CYTOLOGY; ENDOPLASMIC RETICULUM; HUMAN; LIFE; LIPID COMPOSITION; LIPID METABOLISM; LIPID STORAGE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; THEORY; VITAL STATISTICS;

ACYLTRANSFERASES; ANIMALS; HUMANS; LIPID METABOLISM; MEMBRANE FUSION; ORGANELLE SIZE; ORGANELLES; PROTEIN TRANSPORT;

EID: 67349158055     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2008.10.009     Document Type: Review

References (86)

1. Sessa G., and Weissmann G. Phospholipid spherules (liposomes) as a model for biological membranes. J. Lipid Res. 9 (1968) 310-318
2. Guo Y., Walther T., Rao M., Stuurman N., Goshima G., Terayama K., Wong J., Vale R., Walter P., Farese, and Jr. R.V. Functional genomic screen reveals genes involved in lipid droplet formation and utilization. Nature 453 7195 (2008) 657-661 (May 29)
3. Cohen A., Razani B., Schubert W., Williams T., Wang X., Iyengar P., Brasaemle D., Scherer P., and Lisanti M. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 53 (2004) 1261-1270
4. Vance J. Molecular and cell biology of phosphatidylserine and phosphatidylethanolamine metabolism. Prog. Nucleic Acid Res. Mol. Biol. 75 (2003) 69-111
5. Bartz R., Zehmer J., Zhu M., Chen Y., Serrero G., Zhao Y., and Liu P. Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation. J. Proteome Res. 6 (2007) 3256-3265
6. Bartz R., Li W.H., Venables B., Zehmer J.K., Roth M.R., Welti R., Anderson R.G., Liu P., and Chapman K.D. Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic. J. Lipid Res. 48 (2007) 837-847
7. Tauchi-Sato K., Ozeki S., Houjou T., Tagushi R., and Fujimoto T. The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277 (2002) 44507-44512
8. Parton R., and Simons K. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8 (2007) 185-194
9. Ostermeyer A., Paci J., Zeng Y., Lublin D., Munro S., and Brown D. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J. Cell Biol. 152 (2001) 1071-1078
10. Pol A., Luetterforst R., Lindsay M., Heinoo S., Ikonen E., and Parton R. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152 (2001) 1057-1070
11. Fujimoto T., Kogo H., Ishiguro K., Tauchi K., and Nomura R. Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J. Cell Biol. 152 (2001) 1079-1085
12. Glenney J., and Soppet D. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 10517-10521
13. Ostermeyer A., Ramcharan L., Zeng Y., Lublin D., and Brown D. Role of the hydrophobic domain in targeting caveolin-1 to lipid droplets. J. Cell Biol. 164 (2004) 69-78
14. Kuerschner L., Moessinger C., and Thiele C. Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets. Traffic 9 (2008) 338-352
15. Stone S., Levin M., Farese, and Jr. R.V. Membrane topology and identification of key functional amino acid residues of murine acyl-CoA:diacylglycerol acyltransferase-2. J. Biol. Chem. 281 (2006) 40273-40282
16. Londos C., Sztalryd C., Tansey J., and Kimmel A. Role of PAT proteins in lipid metabolism. Biochimie 87 (2005) 45-49
17. Hickenbottom S., Kimmel A., Londos C., and Hurley J. Structure of a lipid droplet protein; the PAT family member TIP47. Structure 12 (2004) 1199-1207
18. Wilson C., Wardell M.R., Weisgraber K.H., Mahley R.W., and Agard D.A. Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E. Science 252 (1991) 1817-1822
19. Lu B., Morrow J.A., and Weisgraber K.H. Conformational reorganization of the four-helix bundle of human apolipoprotein E in binding to phospholipids. J. Biol. Chem. 275 (2000) 20775-20781
20. Wolins N., Quaynor B., Skinner J., Schoenfish M., Tzekov A., and Bickel P. S3-12, adipophilin, and TIP47 package lipid in adipocytes. J. Biol. Chem. 280 (2005) 19146-19155
21. Welte M. Proteins under new management: lipid droplets deliver. Trends Cell Biol. 17 (2007) 363-369
22. Litvak V., Shaul Y., Shulewitz M., Amarilio R., Carmon S., and Lev S. Targeting of Nir2 to lipid droplets is regulated by a specific threonine residue within its PI-transfer domain. Curr. Biol. 12 (2002) 1513-1518
23. Liu P., Ying Y., Zhao Y., Mundy D.I., Zhu M., and Anderson R.G. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279 (2004) 3787-3792
24. Beller M., Riedel D., Jansch L., Dieterich G., Wehland J., Jackle H., and Kuhnlein R.P. Characterization of the Drosophila lipid droplet subproteome. Mol. Cell Proteomics 5 (2006) 1082-1094
25. Cermelli S., Guo Y., Gross S., and Welte M. The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr. Biol. 16 (2006) 1783-1795
26. Wältermann M., Hinz A., Robenek H., Troyer D., Reichelt R., Malkus U., Galla H., Kalscheuer R., Stöveken T., Landenberg P.V., and Steinbüchel A. Mechanism of lipid-body formation in prokaryotes: how bacteria fatten up. Mol. Microbiol. 55 (2005) 750-763
27. Robenek H., Hofnagel O., Buers I., Robenek M.J., Troyer D., and Severs N.J. Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. J. Cell Sci. 119 (2006) 4215-4224
28. Buhman K.K., Chen H.C., Farese, and Jr. R.V. The enzymes of neutral lipid synthesis. J. Biol. Chem. 276 (2001) 40369-40372
29. Lardizabal K.D., Mai J.T., Wagner N.W., Wyrick A., Voelker T., and Hawkins D.J. DGAT2 is a new diacylglycerol acyltransferase gene family. Purification, cloning, and expression in insect cells of two polypeptides from Mortierella ramanniana with diacylglycerol acyltransferase activity. J. Biol. Chem. 276 (2001) 38862-38869
30. Cases S., Stone S.J., Zhou P., Yen E., Tow B., Lardizabal K.D., Voelker T., Farese, and Jr. R.V. Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members. J. Biol. Chem. 276 (2001) 38870-38876
31. Sturmey R., O'Toole P., and Leese H. Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132 (2006) 829-837
32. Blanchette-Mackie E., Dwyer N., Barber T., Coxey R., Takeda T., Rondinone C., Theodorakis J., Greenberg A., and Londos C. Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36 (1995) 1211-1226
33. Goodman J.M. The gregarious lipid droplet. J. Biol Chem. 283 42 (2008) 28005-28009 (Oct 17)
34. Ploegh H. A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature 448 (2007) 435-438
35. Robenek H., Robenek M., and Troyer D. PAT family proteins pervade lipid droplet cores. J. Lipid Res. 46 (2005) 1331-1338
36. Robenek M.J., Severs N.J., Schlattmann K., Plenz G., Zimmer K.P., Troyer D., and Robenek H. Lipids partition caveolin-1 from ER membranes into lipid droplets: Updating the model of lipid droplet biogenesis. Faseb J. 18 (2004) 866-868
37. Nakamura N., Banno Y., and Tamiya-Koizumi K. Arf1-dependent PLD1 is localized to oleic acid-induced lipid droplets in NIH3T3 cells. Biochem. Biophys. Res. Commun. 335 (2005) 117-123
38. Boström P., Andersson L., Rutberg M., Perman J., Lidberg U., Johansson B., Fernandez-Rodriguez J., Ericson J., Nilsson T., Borén J., and Olofsson S. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat. Cell Biol. 9 (2007) 1286-1293
39. Hofmann K. A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trends Biochem. Sci. 25 (2000) 111-112
40. Buhman K.F., Accad M., Farese, and Jr. R.V. Mammalian acyl-CoA:cholesterol acyltransferases. Biochim. Biophys. Acta 1529 (2000) 142-154
41. Yang H., Bard M., Bruner D.A., Gleeson A., Deckelbaum R.J., Aljinovic G., Pohl T.M., Rothstein R., and Sturley S.L. Sterol esterification in yeast: a two-gene process. Science 272 (1996) 1353-1356
42. Sorger D., and Daum G. Synthesis of triacylglycerols by the acyl-coenzyme A:diacyl-glycerol acyltransferase Dga1p in lipid particles of the yeast Saccharomyces cerevisiae. J. Bacteriol. 184 (2002) 519-524
43. Levine T., and Loewen C. Inter-organelle membrane contact sites: through a glass, darkly. Curr. Opin. Cell Biol. 18 (2006) 371-378
44. Schulz T., and Prinz W. Sterol transport in yeast and the oxysterol binding protein homologue (OSH) family. Biochim. Biophys. Acta 1771 (2007) 769-780
45. Hanada K., Kumagai K., Tomishige N., and Kawano M. CERT and intracellular trafficking of ceramide. Biochim. Biophys. Acta 1771 (2007) 644-653
46. Brown R., and Mattjus P. Glycolipid transfer proteins. Biochim. Biophys. Acta 1771 (2007) 746-760
47. Szymanski K., Binns D., Bartz R., Grishin N., Li W., Agarwal A., Garg A., Anderson R., and Goodman J. The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 20890-20895
48. Fei W., Shui G., Gaeta B., Du X., Kuerschner L., Li P., Brown A., Wenk M., Parton R., and Yang H. Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J. Cell Biol. 180 (2008) 473-482
49. Ost A., Ortegren U., Gustavsson J., Nystrom F.H., and Stralfors P. Triacylglycerol is synthesized in a specific subclass of caveolae in primary adipocytes. J. Biol. Chem. 280 (2005) 5-8
50. Brasaemle D.L., Dolios G., Shapiro L., and Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279 (2004) 46835-46842
51. Rajendran L., LeLay S., and Illges H. Raft association and lipid droplet targeting of flotillins are independent of caveolin. Biol. Chem. 388 (2007) 307-314
52. Fernández M., Albor C., Ingelmo-Torres M., Nixon S., Ferguson C., Kurzchalia T., Tebar F., Enrich C., Parton R., and Pol A. Caveolin-1 is essential for liver regeneration. Science 313 (2006) 1628-1632
53. Pohl J., Ring A., and Stremmel W. Uptake of long-chain fatty acids in HepG2 cells involves caveolae: analysis of a novel pathway. J. Lipid Res. 43 (2002) 1390-1399
54. Liu P., Bartz R., Zehmer J., Ying Y., Zhu M., Serrero G., and Anderson R. Rab-regulated interaction of early endosomes with lipid droplets. Biochim. Biophys. Acta 1773 (2007) 784-793
55. Binns D., Januszewski T., Chen Y., Hill J., Markin V., Zhao Y., Gilpin C., Chapman K., Anderson R., and Goodman J. An intimate collaboration between peroxisomes and lipid bodies. J. Cell Biol. 173 (2006) 719-731
56. Hölttä-Vuori M., Tanhuanpää K., Möbius W., Somerharju P., and Ikonen E. Modulation of cellular cholesterol transport and homeostasis by Rab11. Mol. Biol. Cell 13 (2002) 3107-3122
57. Ozeki S., Cheng J., Tauchi-Sato K., Hatano N., Taniguchi H., and Fujimoto T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 118 (2005) 2601-2611
58. Andersson L., Boström P., Ericson J., Rutberg M., Magnusson B., Marchesan D., Ruiz M., Asp L., Huang P., Frohman M., Borén J., and Olofsson S. PLD1 and ERK2 regulate cytosolic lipid droplet formation. J. Cell Sci. 119 (2006) 2246-2257
59. Guo Y., Jangi S., and Welte M. Organelle-specific control of intracellular transport: distinctly targeted isoforms of the regulator Klar. Mol. Biol. Cell 16 (2005) 1406-1416
60. Welte M.A., Cermelli S., Griner J., Viera A., Guo Y., Kim D.H., Gindhart J.G., and Gross S.P. Regulation of lipid-droplet transport by the perilipin homolog LSD2. Curr. Biol. 15 (2005) 1266-1275
61. Savage M., Goldberg D., and Schacher S. Absolute specificity for retrograde fast axonal transport displayed by lipid droplets originating in the axon of an identified Aplysia neuron in vitro. Brain Res. 406 (1987) 215-223
62. Boström P., Rutberg M., Ericsson J., Holmdahl P., Andersson L., Frohman M., Borén J., and Olofsson S. Cytosolic lipid droplets increase in size by microtubule-dependent complex formation. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1945-1951
63. Marchesan D., Rutberg M., Andersson L., Asp L., Larsson T., Borén J., Johansson B., and Olofsson S. A phospholipase D-dependent process forms lipid droplets containing caveolin, adipocyte differentiation-related protein, and vimentin in a cell-free system. J. Biol. Chem. 278 (2003) 27293-27300
64. Marcinkiewicz A., Gauthier D., Garcia A., and Brasaemle D.L. The phosphorylation of serine 492 of perilipin a directs lipid droplet fragmentation and dispersion. J. Biol. Chem. 281 (2006) 11901-11909
65. Zechner R., Strauss J.G., Haemmerle G., Lass A., and Zimmermann R. Lipolysis: pathway under construction. Curr. Opin. Lipidol. 16 (2005) 333-340
66. Sztalryd C., Bell M., Lu X., Mertz P., Hickenbottom S., Chang B., Chan L., Kimmel A., and Londos C. Functional compensation for adipose differentiation-related protein (ADFP) by Tip47 in an ADFP null embryonic cell line. J. Biol. Chem. 281 (2006) 34341-34348
67. Zimmermann R., Strauss J.G., Haemmerle G., Schoiswohl G., Birner-Gruenberger R., Riederer M., Lass A., Neuberger G., Eisenhaber F., Hermetter A., and Zechner R. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306 (2004) 1383-1386
68. Salter A., Wiggins D., Sessions V., and Gibbons G. The intracellular triacylglycerol/fatty acid cycle: a comparison of its activity in hepatocytes which secrete exclusively apolipoprotein (apo) B100 very-low-density lipoprotein (VLDL) and in those which secrete predominantly apoB48 VLDL. Biochem. J. 332 (1998) 667-672
69. Sztalryd C., Xu G., Dorward H., Tansey J., Contreras J., Kimmel A., and Londos C. Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J. Cell. Biol. 161 (2003) 1093-1103
70. Londos C., Brasaemle D., Schultz C., Segrest J., Kimmel A., and Perilipins. ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. Semin. Cell Dev. Biol. 10 (1999) 51-58
71. Köffel R., Tiwari R., Falquet L., and Schneiter R. 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 (2005) 1655-1668
72. Daum G., Wagner A., Czabany T., and Athenstaedt K. Dynamics of neutral lipid storage and mobilization in yeast. Biochimie 89 (2007) 243-248
73. Hope R., and McLauchlan J. Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J. Gen. Virol. 81 (2000) 1913-1925
74. Miyanari Y., Atsuzawa K., Usuda N., Watashi K., Hishiki T., Zayas M., Bartenschlager R., Wakita T., Hijikata M., and Shimotohno K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9 (2007) 1089-1097
75. Shavinskaya A., Boulant S., Penin F., McLauchlan J., and Bartenschlager R. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem. 282 (2007) 37158-37169
76. Kumar Y., Cocchiaro J., and Valdivia R.H. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16 (2006) 1646-1651
77. Cho S., Shin E., Park P., Shin D., Chang H., Kim D., Lee H., Lee J., Kim S., Song M., Chang I., Lee O., and Lee T. Identification of mouse Prp19p as a lipid droplet-associated protein and its possible involvement in the biogenesis of lipid droplets. J. Biol. Chem. 282 (2007) 2456-2465
78. Outeiro T., and Lindquist S. Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 302 (2003) 1772-1775
79. Cole N., Murphy D., Grider T., Rueter S., Brasaemle D., and Nussbaum R. Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein. J. Biol. Chem. 277 (2002) 6344-6352
80. Matsuda D., and Tomoda H. DGAT inhibitors for obesity. Curr. Opin. Investig. Drugs 8 (2007) 836-841
81. Zhao G., Souers A., Voorbach M., Falls H., Droz B., Brodjian S., Lau Y., Iyengar R., Gao J., Judd A., Wagaw S., Ravn M., Engstrom K., Lynch J., Mulhern M., Freeman J., Dayton B.D., Wang X., Grihalde N., Fry D., Beno D., Marsh K., Su Z., Diaz G., Collins C., Sham H., Reilly R., Brune M., and Kym P. Validation of diacyl glycerolacyltransferase I as a novel target for the treatment of obesity and dyslipidemia using a potent and selective small molecule inhibitor. J. Med. Chem. 51 (2008) 380-383
82. Tansey J.T., Sztalryd C., Gruia-Gray J., Roush D.L., Zee J.V., Gavrilova O., Reitman M.L., Deng C.-X., Li C., Kimmel A.R., and Londos C. Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6494-6499
83. Zheng P., Allen W., Roesler K., Williams M., Zhang S., Li J., Glassman K., Ranch J., Nubel D., Solawetz W., Bhattramakki D., Llaca V., Deschamps S., Zhong G., Tarczynski M., and Shen B. A phenylalanine in DGAT is a key determinant of oil content and composition in mice. Nat. Genet. 40 (2008) 367-372
84. Winter A., Kramer W., Werner F.A., Kollers S., Kata S., Durstewitz G., Buitkamp J., Womack J.E., Thaller G., and Fries R. Association of a lysine-232/alanine polymorphism in a bovine gene encoding acyl-CoA:diacylglycerol acyltransferase (DGAT1) with variation at a quantitative trait locus for milk fat content. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9300-9305
85. Schennink A., Stoop W., Visker M., Heck J., Bovenhuis H., Poel J.v.d., Valenberg H.v., and Arendonk J.v. DGAT1 underlies large genetic variation in milk-fat composition of dairy cows. Anim. Genet. 38 (2007) 467-473
86. Heid H., and Keenan T. Intracellular origin and secretion of milk fat globules. Eur. J. Cell Biol. 84 (2005) 245-258