Caveolae and lipid trafficking in adipocytes

Clinical Lipidology

Volumn 6, Issue 1, 2011, Pages 49-58

  Pilch, Paul F ^a   Meshulam, Tova ^a   Ding, Shiying ^a   Liu, Libin ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOSLIN DIABETES CENTER   (United States)

Author keywords

adipocyte; caveolin; cavin; cholesterol; fatty acid; lipid droplet

Indexed keywords

ABC TRANSPORTER A1; CAVEOLIN 1; CAVEOLIN 2; CAVEOLIN 3; CAVIN 1; CAVIN 2; CAVIN 3; CAVIN 4; CHOLESTEROL; FATTY ACID; FATTY ACID TRANSPORTER; FLOTILLIN 1; FLOTILLIN 2; LIPID; MEMBRANE PROTEIN; SPHINGOLIPID; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; CAVEOLA; CELL SPECIFICITY; CELL STRUCTURE; CHOLESTEROL METABOLISM; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID COMPOSITION; LIPID STORAGE; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 79951503693     PISSN: 17460875     EISSN: None     Source Type: Journal    
DOI: 10.2217/clp.10.80     Document Type: Review

References (107)

1. Palade GE: Fine structure of blood capillaries. J. Appl. Physics 24, 1424 (1953).
2. Yamada E: The fne structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1, 445-458 (1955).
3. Parton RG, Simons K: The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8, 185-194 (2007).
4. 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. 127, 1233-1243 (1994). (Pubitemid 24362559)
5. Kandror K V, Stephens JM, Pilch PF: Expression and compartmentalization of caveolin in adipose cells: coordinate regulation with and structural segregation from GLUT4. J. Cell Biol. 129, 999-1006 (1995).
6. Voldstedlund M, Tranum-Jensen J, Vinten J: Quantitation of Na+/K+-ATPase and glucose transporter isoforms in rat adipocyte plasma membrane by immunogold labeling. J. Memb. Biol. 136, 63-73 (1993). (Pubitemid 23312082)
7. Thorn H, Stenkula KG, Karlsson M et al.: Cell surface orifces of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Mol. Biol. Cell 14, 3967-3976 (2003). (Pubitemid 37186301)
8. Tuma PL, Hubbard AL: Transcytosis: crossing cellular barriers. Physiol. Rev. 83, 871-932 (2003). (Pubitemid 36833216)
9. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B: Caveolae are highly immobile plasma membrane m icr odomains, which are not involved in constitutive endocytic traffcking. Mol. Biol. Cell 13, 238-250 (2002). (Pubitemid 34106072)
10. Doherty GJ, McMahon HT: Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902 (2009).
11. Smart EJ, Graf GA, McNiven MA et al.: Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell Biol. 19, 7289-7304 (1999). (Pubitemid 29493393)
12. Bastiani M, Parton RG: Caveolae at a glance. J. Cell Sci. 123, 3831-3836 (2010).
13. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG: Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682 (1992).
14. Aoki S, Thomas A, Decaffmeyer M, Brasseur R, Epand RM: The role of proline in the membrane re-entrant helix of caveolin-1. J. Biol. Chem. 285(43), 33371-33380 (2010).
15. Schmid SL: Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548 (1997). (Pubitemid 27274666)
16. Hansen CG, Nichols BJ: Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol. 20, 177-186 (2010).
17. Fra AM, Williamson E, Simons K, Parton RG: De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl Acad. Sci. USA 92, 8655-8659 (1995).
18. Parolini I, Sargiacomo M, Galbiati F et al.: Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the Golgi complex. J. Biol. Chem. 274, 25718-25725 (1999).
19. Williams TM, Lisanti MP: The caveolin proteins. Genome Biol. 5, 214 (2004).
20. Monier S, Dietzen DJ, Hastings WR, Lublin DM, Kurzchalia TV: Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388, 143-149 (1996). (Pubitemid 26226349)
21. Das K, Lewis RY, Scherer PE, Lisanti MP: The membrane-spanning domains of caveolins-1 and-2 mediate the formation of caveolin hetero-oligomers. Implications for the assembly of caveolae membranes in vivo. J. Biol. Chem. 274, 18721-18728 (1999).
22. Fernandez I, Ying Y, Albanesi J, Anderson RG: Mechanism of caveolin flament assembly. Proc. Natl Acad. Sci. USA 99, 11193-11198 (2002).
23. Liu L, Pilch PF: A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J. Biol. Chem. 283, 4314-4322 (2008).
24. Hill MM, Bastiani M, Luetterforst R et al.: PTRF-cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132, 113-124 (2008).
25. Liu L, Brown D, McKee M et al.: Deletion of cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab. 8, 310-317 (2008).
26. McMahon KA, Zajicek H, Li WP et al.: SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J. 28, 1001-1015 (2009).
27. Hansen CG, Bright NA, Howard G, Nichols BJ: SDPR induces membrane curvature and functions in the formation of caveolae. Nat. Cell Biol. 11, 807-814 (2009).
28. Bastiani M, Liu L, Hill MM et al.: MURC/cavin-4 and cavin family members form tissue-specifc caveolar complexes. J. Cell Biol. 185, 1259-1273 (2009).
29. Ogata T, Ueyama T, Isodono K et al.: MURC, a muscle-restricted coiled-coil protein that modulates the Rho/ROCK pathway, induces cardiac dysfunction and conduction disturbance. Mol. Cell Biol. 28, 3424-3436 (2008). (Pubitemid 351657104)
30. Ikezu T, Ueda H, Trapp BD et al.: Affnity-purifcation and characterization of caveolins from the brain: differential expression of caveolin-1,-2, and-3 in brain endothelial and astroglial cell types. Brain Res. 804, 177-192 (1998). (Pubitemid 28496622)
31. Mineo C, Ying YS, Chapline C, Jaken S, Anderson RG: Targeting of protein kinase Ca to caveolae. J. Cell Biol. 141, 601-610 (1998).
32. Vinten J, Voldstedlund M, Clausen H, Christiansen K, Carlsen J, Tranum-Jensen J: A 60-kDa protein abundant in adipocyte caveolae. Cell Tissue Res. 305, 99-106 (2001). (Pubitemid 32681872)
33. Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J: Identifcation of a major protein on the cytosolic face of caveolae. Biochim. Biophys. Acta 1717, 34-40 (2005). (Pubitemid 41642663)
34. Aboulaich N, Vainonen JP, Stralfors P, Vener AV: Vectorial proteomics reveal targeting, phosphorylation and specifc fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem. J. 383, 237-248 (2004). (Pubitemid 39446684)
35. Jansa P, Mason SW, Hoffmann-Rohrer U, Grummt I: Cloning and functional characterization of PTRF, a novel protein which induces dissociation of paused ternary transcription complexes. EMBO J. 17, 2855-2864 (1998). (Pubitemid 28227132)
36. Gustincich S, Schneider C: Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell Growth Differ. 4, 753-760 (1993).
37. Izumi Y, Hirai S, Tamai Y, Fujise-Matsuoka A, Nishimura Y, Ohno S: A protein kinase Cd-binding protein SRBC whose expression is induced by serum starvation. J. Biol. Chem. 272, 7381-7389 (1997). (Pubitemid 27166449)
38. Hayer A, Stoeber M, Bissig C, Helenius A: Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffc 11, 361-382 (2010).
39. Cushman SW: Structure-function relationships in the adipose cell. I. Ultrastructure of the isolated adipose cell. J. Cell Biol. 46, 326-341 (1970).
40. Carpentier JL, Perrelet A, Orci L: Effects of insulin, glucagon, and epinephrine on the plasma membrane of the white adipose cell: a freeze-fracture study. J. Lipid Res. 17, 335-342 (1976).
41. Guilherme A, Virbasius JV, Puri V, Czech MP: Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 367-377 (2008). (Pubitemid 351574198)
42. Pilch PF, Souto RP, Liu L et al.: Cellular spelunking: exploring adipocyte caveolae. J. Lipid Res. 48, 2103-2111 (2007). (Pubitemid 47529553)
43. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia T V, Simons K: VIP21/caveolin is a cholesterol-binding protein. Proc. Natl Acad. Sci. USA 92, 10339-10343 (1995).
44. Fielding CJ, Bist A, Fielding PE: Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fbroblast monolayers. Proc. Natl Acad. Sci. USA 94, 3753-3758 (1997).
45. Ortegren U, Karlsson M, Blazic N et al.: Lipids and glycosphingolipids in caveolae and surrounding plasma membrane of primary rat adipocytes. Eur. J. Biochem. 271, 2028-2036 (2004). (Pubitemid 38657355)
46. Ridgway ND: Interactions between metabolism and intracellular distribution of cholesterol and sphingomyelin. Biochim. Biophys. Acta 1484, 129-141 (2000). (Pubitemid 30175963)
47. Ikonen E, Heino S, Lusa S: Caveolins and membrane cholesterol. Biochem. Soc. Trans. 32, 121-123 (2004). (Pubitemid 38283029)
48. Cheng ZJ, Singh RD, Marks DL, Pagano RE: Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol. Membr. Biol. 23, 101-110 (2006).
49. Gustincich S, Vatta P, Goruppi S et al.: The human serum deprivation response gene (SDPR) maps to 2q32-q33 and codes for a phosphatidylserine-binding protein. Genomics 57, 120-129 (1999). (Pubitemid 29187944)
50. Garner AE, Smith DA, Hooper NM: Visualization of detergent solubilization of membranes: implications for the isolation of rafts. Biophys. J. 94, 1326-1340 (2008).
51. Lingwood D, Kaiser HJ, Levental I, Simons K: Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37, 955-960 (2009).
52. Brown DA: Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21, 430-439 (2006). (Pubitemid 44879252)
53. Bauer M, Pelkmans L: A new paradigm for membrane-organizing and-shaping scaffolds. FEBS Lett. 580, 5559-5564 (2006). (Pubitemid 44465913)
54. Souto RP, Vallega G, Wharton J, Vinten J, Tranum-Jensen J, Pilch PF: Immunopurifcation and characterization of rat adipocyte caveolae suggest their dissociation from insulin signaling. J. Biol. Chem. 278, 18321-18329 (2003). (Pubitemid 36799452)
55. Frick M, Bright NA, Riento K, Bray A, Merrifed C, Nichols BJ: Coassembly of fotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr. Biol. 17, 1151-1156 (2007). (Pubitemid 46990891)
56. Ikonen E: Cellular cholesterol traffcking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138 (2008).
57. Brown MS, Goldstein JL: Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL. J. Lipid Res. 50(Suppl.), S15-S27 (2009).
58. Mesmin B, Maxfeld FR: Intracellular sterol dynamics. Biochim. Biophys. Acta 1791, 636-645 (2009).
59. Martin S, Parton RG: Caveolin, cholesterol, and lipid bodies. Semin. Cell Dev. Biol. 16, 163-174 (2005). (Pubitemid 40432118)
60. Hailstones D, Sleer LS, Parton RG, Stanley KK: Regulation of caveolin and caveolae by cholesterol in MDCK cells. J. Lipid Res. 39, 369-379 (1998). (Pubitemid 28100674)
61. Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS: Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab. 8, 512-521 (2008).
62. Meshulam T, Simard JR, Wharton J, Hamilton JA, Pilch PF: Role of caveolin-1 and cholesterol in transmembrane fatty acid movement. Biochemistry 45, 2882-2893 (2006). (Pubitemid 43334537)
63. Krause BR, Hartman AD: Adipose tissue and cholesterol metabolism. J. Lipid Res. 25, 97-110 (1984). (Pubitemid 14150090)
64. Kraemer FB, Laane C, Park B, Sztalryd C: Low-density lipoprotein receptors in rat adipocytes: regulation with fasting. Am. J. Physiol. 266, E26-E32 (1994).
65. Le Lay S, Ferre P, Dugail I: Adipocyte cholesterol balance in obesity. Biochem. Soc. Trans. 32, 103-106 (2004). (Pubitemid 38283024)
66. Le Lay S, Hajduch E, Lindsay MR et al.: Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffc 7, 549-561 (2006). (Pubitemid 44026753)
67. Schreibman PH, Dell RB: Human adipocyte cholesterol. Concentration, localization, synthesis, and turnover. J. Clin. Invest. 55, 986-993 (1975).
68. Murphy S, Martin S, Parton RG: Lipid droplet-organelle interactions; sharing the fats. Biochim. Biophys. Acta 1791, 441-447 (2009).
69. Gomez-Ruiz A, Milagro FI, Campion J, Martinez JA, de Miguel C: Caveolin expression and activation in retroperitoneal and subcutaneous adipocytes: infuence of a high-fat diet. J. Cell Physiol. 225, 206-213 (2010).
70. Kozak LP, Newman S, Chao PM, Mendoza T, Koza RA: The early nutritional environment of mice determines the capacity for adipose tissue expansion by modulating genes of caveolae structure. PLoS One 5, E11015 (2010).
71. Le Lay S, Robichon C, Le Liepvre X, Dagher G, Ferre P, Dugail I: Regulation of ABCA1 expression and cholesterol effux during adipose differentiation of 3T3-L1 cells. J. Lipid Res. 44, 1499-1507 (2003). (Pubitemid 37279594)
72. Attie AD: ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends Biochem. Sci. 32, 172-179 (2007). (Pubitemid 46603277)
73. Fielding PE, Russel JS, Spencer TA, Hakamata H, Nagao K, Fielding CJ: Sterol effux to apolipoprotein A-I originates from caveolin-rich microdomains and potentiates PDGF-dependent protein kinase activity. Biochemistry 41, 4929-4937 (2002). (Pubitemid 34298660)
74. Lin YC, Ma C, Hsu WC, Lo HF, Yang VC: Molecular interaction between caveolin-1 and ABCA1 on high-density lipoprotein-mediated cholesterol effux in aortic endothelial cells. Cardiovasc. Res. 75, 575-583 (2007). (Pubitemid 47080965)
75. McMahon KA, Zhu M, Kwon SW, Liu P, Zhao Y, Anderson RG: Detergent-free caveolae proteome suggests an interaction with ER and mitochondria. Proteomics 6, 143-152 (2006). (Pubitemid 43142941)
76. Davalos A, Fernandez-Hernando C, Sowa G et al.: Quantitative proteomics of caveolin-1 regulated proteins: characterization of PTRF/cavin-1 in endothelial cells. Mol. Cell Proteomics 9(10), 2109-2124 (2010).
77. Plutzky J: Expansion and contraction: the mighty, mighty fatty acid. Nat. Med. 15, 618-619 (2009).
78. Fielding BA, Frayn KN: Lipoprotein lipase and the disposition of dietary fatty acids. Br. J. Nutr. 80, 495-502 (1998). (Pubitemid 29060530)
79. Simard JR, Zunszain PA, Ha CE et al.: Locating high-affnity fatty acid-binding sites on albumin by x-ray crystallography and NMR spectroscopy. Proc. Natl Acad. Sci. USA 102, 17958-17963 (2005). (Pubitemid 41798484)
80. Su X, Abumrad NA: Cellular fatty acid uptake: a pathway under construction. Trends Endocrinol. Metab. 20, 72-77 (2009).
81. Hamilton JA: Fast fip-fop of cholesterol and fatty acids in membranes: implications for membrane transport proteins. Curr. Opin. Lipidol. 14, 263-271 (2003). (Pubitemid 36688205)
82. Kampf JP, Parmley D, Kleinfeld AM: Free fatty acid transport across adipocytes is mediated by an unknown membrane protein pump. Am. J. Physiol. Endocrinol. Metab. 293, E1207-E1214 (2007). (Pubitemid 350106586)
83. Mashek DG, Coleman RA: Cellular fatty acid uptake: the contribution of metabolism. Curr. Opin. Lipidol. 17, 274-278 (2006). (Pubitemid 43786061)
84. Pohl J, Ring A, Hermann T, Stremmel W: Role of FATP in parenchymal cell fatty acid uptake. Biochim. Biophys. Acta 1686, 1-6 (2004). (Pubitemid 39446872)
85. Kandror KV, Pilch PF: gp160, a tissue-specifc marker for insulin-activated glucose transport. Proc. Natl Acad. Sci. USA 91, 8017-8021 (1994). (Pubitemid 24253877)
86. Trigatti BL, Anderson RG, Gerber GE: Identifcation of caveolin-1 as a fatty acid binding protein. Biochem. Biophys. Res. Commun. 255, 34-39 (1999). (Pubitemid 29292060)
87. Kamp F, Hamilton JA: pH gradients across phospholipid membranes caused by fast fip-fop of un-ionized fatty acids. Proc. Natl Acad. Sci. USA 89, 11367-11370 (1992).
88. Simard JR, Meshulam T, Pillai BK et al.: Caveolins sequester FA on the cytoplasmic leafet of the plasma membrane, augment triglyceride formation, and protect cells from lipotoxicity. J. Lipid Res. 51, 914-922 (2010).
89. Stralfors P: Autolysis of isolated adipocytes by endogenously produced fatty acids. FEBS Lett. 263, 153-154 (1990). (Pubitemid 20107800)
90. Ost A, Ortegren U, Gustavsson J, Nystrom FH, Stralfors P: Triacylglycerol is synthesized in a specifc subclass of caveolae in primary adipocytes. J. Biol. Chem. 280, 5-8 (2005). (Pubitemid 40164958)
91. Razani B, Combs TP, Wang XB et al.: Caveolin-1-defcient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277, 8635-8647 (2002). (Pubitemid 34968330)
92. Cao H, Alston L, Ruschman J, Hegele RA: Heterozygous Cav1 frameshift mutations (MIM 601047) in patients with atypical partial lipodystrophy and hypertriglyceridemia. Lipids Health Dis. 7, 3 (2008).
93. Kim CA, Delepine M, Boutet E et al.: Association of a homozygous nonsense caveolin-1 mutation with Berardinelli-Seip congenital lipodystrophy. J. Clin. Endocrinol. Metab. 93, 1129-1134 (2008). (Pubitemid 351540679)
94. Hayashi YK, Matsuda C, Ogawa M et al.: Human PTRF mutations cause secondary defciency of caveolins resulting in muscular dystrophy with generalized lipodystrophy J. Clin. Invest. 119, 2623-2633 (2009).
95. Rajab A, Straub V, McCann LJ et al.: Fatal cardiac arrhythmia and long-QT syndrome in a new form of congenital generalized lipodystrophy with muscle rippling (CGL4) due to PTRF-cavin mutations. PLoS Genet. 6, E1000874 (2010).
96. Dwianingsih EK, Takeshima Y, Itoh K et al.: A Japanese child with asymptomatic elevation of serum creatine kinase shows PTRF-cavin mutation matching with congenital generalized lipodystrophy type 4. Mol. Genet. Metab. 101, 233-237 (2010).
97. Shastry S, Delgado MR, Dirik E, Turkmen M, Agarwal AK, Garg A: Congenital generalized lipodystrophy, type 4 (CGL4) associated with myopathy due to novel PTRF mutations. Am. J. Med. Genet. A 152A, 2245-2253 (2010).
98. Le Lay S, Briand N, Blouin CM et al.: The lipoatrophic caveolin-1 defcient mouse model reveals autophagy in mature adipocytes. Autophagy 6, 754-763 (2010).
99. Kamp F, Guo W, Souto R, Pilch PF, Corkey BE, Hamilton JA: Rapid fip-fop of oleic acid across the plasma membrane of adipocytes. J. Biol. Chem. 278, 7988-7995 (2003). (Pubitemid 36800537)
100. 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. 279, 46835-46842 (2004). (Pubitemid 39518334)
101. Cohen AW, Razani B, Schubert W et al.: Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 53, 1261-1270 (2004). (Pubitemid 38569012)
102. 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 traffc. J. Biol. Chem. 279, 3787-3792 (2004). (Pubitemid 38140623)
103. Robenek MJ, Severs NJ, Schlattmann K et al.: Lipids partition caveolin-1 from ER membranes into lipid droplets: updating the model of lipid droplet biogenesis. FASEB J. 18, 866-868 (2004).
104. Jedrychowski MP, Gartner CA, Gygi SP et al.: Proteomic analysis of GLUT4 storage vesicles reveals LRP1 to be an important vesicle component and target of insulin signaling. J. Biol. Chem. 285, 104-114 (2010).
105. 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. 152, 1071-1078 (2001). (Pubitemid 34286081)
106. Pol A, Martin S, Fernandez MA, Ingelmo-Torres M et al.: Cholesterol and fatty acids regulate dynamic caveolin traffcking through the Golgi complex and between the cell surface and lipid bodies. Mol. Biol. Cell 16, 2091-2105 (2005). (Pubitemid 40471974)
107. Ortegren U, Yin L, Ost A, Karlsson H, Nystrom FH, Stralfors P: Separation and characterization of caveolae subclasses in the plasma membrane of primary adipocytes: segregation of specifc proteins and functions. FEBS J. 273, 3381-3392 (2006). (Pubitemid 43990939)