Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: A role for caveolar endocytosis

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Volumn 7, Issue 5, 2006, Pages 549-561

  Le Lay, Soazig ^a   Hajduch, Eric ^b,c   Lindsay, Margaret R ^d   Le Lièpvre, Xavier ^b,c   Thiele, Christoph ^a   Ferré, Pascal ^b,c   Parton, Robert G ^d   Kurzchalia, Teymuras ^a   Simons, Kai ^a   Dugail, Isabelle ^b,c  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adipocyte; Caveolin; Cholesterol; Endocytosis; Lipid droplets; Protein traffic

Indexed keywords

CAVEOLIN; CAVEOLIN 1; CHOLESTEROL; DYNAMIN; FAT DROPLET; PROTEIN KINASE C; PROTEIN KINASE P60;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL COMPOSITION; CELL FRACTIONATION; CELL ORGANELLE; CELL STRAIN 3T3; CONTROLLED STUDY; ENDOCYTOSIS; INTRACELLULAR TRANSPORT; KNOCKOUT MOUSE; MALE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CAVEOLAE; CAVEOLIN 1; CHOLESTEROL; ENDOCYTOSIS; MALE; MICE; MICE, KNOCKOUT;

EID: 33745844829     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2006.00406.x     Document Type: Article

References (72)

1. Fujimoto T, Kogo H, Ishiguro K, Tauchi K, Nomura R. Caveolin-2 is targeted to lipid droplets, a new 'membrane domain'in the cell. J Cell Biol 2001;152:1079-1085.
2. Londos C, Sztalryd C, Tansey JT, Kimmel AR. Role of PAT proteins in lipid metabolism. Biochimie 2005;87:45-49.
3. Brasaemle DL, Dolios G, Shapiro L, Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J Biol Chem 2004;279:46835-46842.
4. Fujimoto Y, Itabe H, Sakai J, Makita M, Noda J, Mori M, Higashi Y, Kojima S, Takano T. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim Biophys Acta 2004;1644:47-59.
5. Liu P, Ying Y, Zhao Y, Mundy DI, Zhu M, Anderson RG. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J Biol Chem 2004;279:3787-3792.
6. Umlauf E, Csaszar E, Moertelmaier M, Schuetz GJ, Parton RG, Prohaska R. Association of stomatin with lipid bodies. J Biol Chem 2004;279:23699-23709.
7. Ostermeyer AG, Paci JM, Zeng Y, Lublin DM, Munro S, Brown DA. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J Cell Biol 2001;152:1071-1078.
8. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, Parton RG. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 2001;152:1057-1070.
9. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 1995;92:10339-10343.
10. Trigatti BL, Anderson RG, Gerber GE. Identification of caveolin-1 as a fatty acid binding protein. Biochem Biophys Res Commun 1999;255:34-39.
11. Ikonen E, Heino S, Lusa S. Caveolins and membrane cholesterol. Biochem Soc Trans 2004;32:121-123.
12. Martin S, Parton RG. Caveolin, cholesterol, and lipid bodies. Semin Cell Dev Biol 2005;16:163-174.
13. Pol A, Martin S, Fernandez MA, Ferguson C, Carozzi A, Luetterforst R, Enrich C, Parton RG. Dynamic and regulated association of caveolin with lipid bodies: Modulation of lipid body motility and function by a dominant negative mutant. Mol Biol Cell 2004;15:99-110.
14. Scherer PE, Lisanti MP, Baldini G, Sargiacomo M, Mastick CC, Lodish HF. Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J Cell Biol 1994;127:1233-1243.
15. Miettinen TA, Tilvis RS. Cholesterol synthesis and storage in adipose tissue. Int J Obes 1981;5:613-618.
16. Kovanen PT, Nikkila EA, Miettinen TA. Regulation of cholesterol synthesis and storage in fat cells. J Lipid Res 1975;16:211-223.
17. Prattes S, Horl G, Hammer A, Blaschitz A, Graier WF, Sattler W, Zechner R, Steyrer E. Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: Triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures. J Cell Sci 2000;113:2977-2989.
18. Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T. The surface of lipid droplets is a phospholipid monolayer with a unique Fatty Acid composition. J Biol Chem 2002;277:44507-44512.
19. Wang X, Sato R, Brown MS, Hua X, Goldstein JL. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 1994;77:53-62.
20. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2000;2:42-49.
21. Uittenbogaard A, Ying Y, Smart EJ. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J Biol Chem 1998;273:6525-6532.
22. Pelkmans L, Helenius A. Endocytosis via caveolae. Traffic 2002;3:311-320.
23. Nichols B. Caveosomes and endocytosis of lipid rafts. J Cell Sci 2003;116:4707-4714.
24. De Camilli P, Takei K, McPherson PS. The function of dynamin in endocytosis. Curr Opin Neurobiol 1995;5:559-565.
25. Fish KN, Schmid SL, Damke H. Evidence that dynamin-2 functions as a signal-transducing GTPase. J Cell Biol 2000;150:145-154.
26. Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol 1994;127:1199-1215.
27. Sharma DK, Brown JC, Choudhury A, Peterson TE, Holicky E, Marks DL, Simari R, Parton RG, Pagano RE. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol Biol Cell 2004;15:3114-3122.
28. Smart EJ, Ying YS, Anderson RG. Hormonal regulation of caveolae internalization. J Cell Biol 1995;131:929-938.
29. Powell DJ, Hajduch E, Kular G, Hundal HS. Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism. Mol Cell Biol 2003;23:7794-7808.
30. Minshall RD, Tiruppathi C, Vogel SM, Niles WD, Gilchrist A, Hamm HE, Malik AB. Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i) -coupled Src kinase signaling pathway. J Cell Biol 2000;150:1057-1070.
31. Harris KF, Shoji I, Cooper EM, Kumar S, Oda H, Howley PM. Ubiquitin-mediated degradation of active Src tyrosine kinase. Proc Natl Acad Sci USA 1999;96:13738-13743.
32. Souto RP, Vallega G, Wharton J, Vinten J, Tranum-Jensen J, Pilch PF. Immunopurification and characterization of rat adipocyte caveolae suggest their dissociation from insulin signaling. J Biol Chem 2003;278:18321-18329.
33. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005;168:465-476.
34. Matveev S, Uittenbogaard A, van Der Westhuyzen D, Smart EJ. Caveolin-1 negatively regulates SR-BI mediated selective uptake of high-density lipoprotein-derived cholesteryl ester. Eur J Biochem 2001;268:5609-5616.
35. Fielding PE, Fielding CJ. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry 1995;34:14288-14292.
36. Frank PG, Galbiati F, Volonte D, Razani B, Cohen DE, Marcel YL, Lisanti MP. Influence of caveolin-1 on cellular cholesterol efflux mediated by high-density lipoproteins. Am J Physiol Cell Physiol 2001;280:C1204-C1214.
37. Fielding PE, Russel JS, Spencer TA, Hakamata H, Nagao K, Fielding CJ. Sterol efflux to apolipoprotein A-I originates from caveolin-rich microdomains and potentiates PDGF-dependent protein kinase activity. Biochemistry 2002;41:4929-4937.
38. Fu Y, Hoang A, Escher G, Parton RG, Krozowski Z, Sviridov D. Expression of caveolin-1 enhances cholesterol efflux in hepatic cells. J Biol Chem 2004;279:14140-14146.
39. Lusa S, Heino S, Ikonen E. Differential mobilization of newly synthesized cholesterol and biosynthetic sterol precursors from cells. J Biol Chem 2003;278:19844-19851.
40. Uittenbogaard A, Smart EJ. Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem 2000;275:25595-25599.
41. Pike LJ, Han X, Chung KN, Gross RW. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: A quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 2002;41:2075-2088.
42. Cohen AW, Razani B, Schubert W, Williams TM, Wang XB, Iyengar P, Brasaemle DL, Scherer PE, Lisanti MP. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 2004;53:1261-1270.
43. Pol A, Martin S, Fernandez MA, Ingelmo-Torres M, Ferguson C, Enrich C, Parton RG. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol Biol Cell 2005;16:2091-2105.
44. Uittenbogaard A, Everson WV, Matveev SV, Smart EJ. Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J Biol Chem 2002;277:4925-4931.
45. Angel A, Farkas J. Regulation of cholesterol storage in adipose tissue. J Lipid Res 1974;15:491-499.
46. Parton RG, Richards AA. Lipid rafts and caveolae as portals for endocytosis: New insights and common mechanisms. Traffic 2003;4:724-738.
47. Anderson HA, Chen Y, Norkin LC. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell 1996;7:1825-1834.
48. Pelkmans L, Puntener D, Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002;296:535-539.
49. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E, Zerial M. Genome-wide analysis of human kinases in clathrin- and caveolae/ raft-mediated endocytosis. Nature 2005;436:78-86.
50. Le PU, Nabi IR. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 2003;116:1059-1071.
51. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001;3:473-483.
52. Parton RG, Molero JC, Floetenmeyer M, Green KM, James DE. Characterization of a distinct plasma membrane macrodomain in differentiated adipocytes. J Biol Chem 2002;277:46769-46778.
53. Kanzaki M, Pessin JE. Caveolin-associated filamentous actin (Cav-actin) defines a novel F-actin structure in adipocytes. J Biol Chem 2002;277:25867-25869.
54. Ost A, Ortegren U, Gustavsson J, Nystrom FH, Stralfors P. Triacylglycerol is synthesized in a specific subclass of caveolae in primary adipocytes. J Biol Chem 2005;280:5-8.
55. Blanchette-Mackie EJ, Dwyer NK, Barber T, Coxey RA, Takeda T, Rondinone CM, Theodorakis JL, Greenberg AS, Londos C. Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J Lipid Res 1995;36:1211-1226.
56. Martin S, Driessen K, Nixon SJ, Zerial M, Parton RG. Regulated localization of Rab18 to lipid droplets: Effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J Biol Chem 2005;280:42325-42335.
57. Ozeki S, Cheng J, Tauchi-Sato K, Hatano N, Taniguchi H, Fujimoto T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 2005;118:2601-2611.
58. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell RG, Li M, Tang B, Jelicks LA, Scherer PE, Lisanti MP. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem 2002;277:8635-8647.
59. Le Lay S, Kurzchalia TV. Getting rid of caveolins: Phenotypes of caveolin-deficient animals. Biochim Biophys Acta 2005;1746:322-333.
60. Le Lay S, Krief S, Farnier C, Lefrere I, Le Liepvre X, Bazin R, Ferre P, Dugail I. Cholesterol, a cell size-dependent signal that regulates glucose metabolism and gene expression in adipocytes. J Biol Chem 2001;276:16904-16910.
61. Friedman JM. Obesity in the new millennium. Nature 2000;404:632-634.
62. Storch J, Shulman SL, Kleinfeld AM. Plasma membrane lipid order and composition during adipocyte differentiation of 3T3F442A cells. Studies in intact cells with 1-[4-(trimethylamino) phenyl]-6-phenylhexatriene. J Biol Chem 1989;264:10527-10533.
63. Guerre-Millo M, Guesnet P, Guichard C, Durand G, Lavau M. Alteration in membrane lipid order and composition in metabolically hyperactive fatty rat adipocytes. Lipids 1994;29:205-209.
64. Schreibman PH, Dell RB. Human adipocyte cholesterol. Concentration, localization, synthesis, and turnover. J Clin Invest 1975;55:986-993.
65. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001;293:2449-2452.
66. Altschuler Y, Barbas SM, Terlecky LJ, Tang K, Hardy S, Mostov KE, Schmid SL. Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J Cell Biol 1998;143:1871-1881.
67. Le Lay S, Lefrere I, Trautwein C, Dugail I, Krief S. Insulin and sterol-regulatory element-binding protein-1c (SREBP-1C) regulation of gene expression in 3T3-L1 adipocytes. Identification of CCAAT/ enhancer-binding protein beta as an SREBP-1C target. J Biol Chem 2002;277:35625-35634.
68. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998;95:2509-2514.
69. Hajduch E, Aledo JC, Watts C, Hundal HS. Proteolytic cleavage of cellubrevin and vesicle-associated membrane protein (VAMP) by tetanus toxin does not impair insulin-stimulated glucose transport or GLUT4 translocation in rat adipocytes. Biochem J 1997;321:233-238.
70. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
71. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509.
72. Tabas I, Zha X, Beatini N, Myers JN, Maxfield FR. The actin cytoskeleton is important for the stimulation of cholesterol esterification by atherogenic lipoproteins in macrophages. J Biol Chem 1994;269:22547-22556.