Caveolin-1 loss of function accelerates glucose transporter 4 and insulin receptor degradation in 3T3-L1 adipocytes

Endocrinology

Volumn 150, Issue 8, 2009, Pages 3493-3502

  González Muñoz, Elena ^a   López Iglesias, Carmen ^a   Calvo, Maria ^a   Palacín, Manuel ^a   Zorzano, Antonio ^a,b   Camps, Marta ^a,b,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Departament de Fisiologia i Immunologia (Biologia)   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CHOLERA TOXIN; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR; LENTIVIRUS VECTOR; SMALL INTERFERING RNA;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CAVEOLA; CELL DIFFERENTIATION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; GENE EXPRESSION; GLUCOSE TRANSPORT; INSULIN DEGRADATION; LIPID RAFT; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN DEGRADATION; RNA INTERFERENCE;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; BIOLOGICAL TRANSPORT; CAVEOLAE; CAVEOLIN 1; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TRANSPORTER TYPE 4; HYPOGLYCEMIC AGENTS; IMMUNOPRECIPITATION; INSULIN; LENTIVIRUS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; RECEPTOR, INSULIN; RNA, SMALL INTERFERING;

EID: 67651183872     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1520     Document Type: Article

References (65)

1. Simons K, Ikonen E 1997 Functional rafts in cell membranes. Nature 387: 569-572
2. van Deurs B, Roepstorff K, Hommelgaard AM, Sandvig K 2003 Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol 13: 92-100
3. Fan JY, Carpentier JL, van Obberghen E, Grunfeld C, Gorden P, Orci L 1983 Morphological changes of the 3T3-L1 fibroblast plasma membrane upon differentiation to the adipocyte form. J Cell Sci 61:219-230
4. Scherer PE, Lisanti MP, Baldini G, Sargiacomo M, Mastick CC, Lodish HF 1994 Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J Cell Biol 127:1233-1243
5. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell RG, Li M, Tang B, Jelicks LA, Scherer PE, Lisanti MP 2002 Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem 277:8635-8647
6. Cao H, Alston L, Ruschman J, Hegele RA 2008 Heterozygous CAV1 frameshift mutations (MIM 601047) in patients with atypical partial lipodystrophy and hypertriglyceridemia. Lipids Health Dis 7:3
7. Kim CA, DelépineM, Boutet E, El Mourabit H, Le Lay S, Meier M, Nemani M, Bridel E, Leite CC, Bertola DR, Semple RK, O'Rahilly S, Dugail I, Capeau J, Lathrop M, MagréJ 2008 Association of a homozygous nonsense caveolin-1 mutation with Berardinelli-Seip congenital lipodystrophy. J Clin Endocrinol Metab 93:1129-1134
8. Catalan V, Gomez-Ambrosi J, Rodriguez A, Silva C, Rotellar F, Gil MJ, Cienfuegos JA, Salvador J, Fruhbeck G 2008 Expression of caveolin-1 in human adipose tissue is upregulated in obesity and obesity-associated type 2 diabetes mellitus and related to inflammation. Clin Endocrinol (Oxf) 68:213-219
9. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, Hancock JF, Parton RG 2008 PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132:113-124
10. Liu L, Pilch PF 2008 A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 283:4314-4322
11. Liu L, Brown D, McKee M, Lebrasseur NK, Yang D, Albrecht KH, Ravid K, Pilch PF 2008 Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab 8:310-317
12. Cohen AW, Combs TP, Scherer PE, Lisanti MP 2003 Role of caveolin and caveolae in insulin signaling and diabetes. Am J Physiol Endocrinol Metab 285:E1151-E1160
13. Cohen AW, Razani B, Wang XB, Combs TP, Williams TM, Scherer PE, Lisanti MP 2003 Caveolin-1-deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am J Physiol Cell Physiol 285:C222-C235
14. Nystrom FH, Chen H, Cong LN, Li Y, Quon MJ 1999 Caveolin-1 interacts with the insulin receptor and can differentially modulate insulin signaling in transfected Cos-7 cells and rat adipose cells. Mol Endocrinol 13:2013-2024
15. Yamamoto M, Toya Y, Schwencke C, Lisanti MP, Myers Jr MG, Ishikawa Y 1998 Caveolin is an activator of insulin receptor signaling. J Biol Chem 273: 26962-26968
16. Baumann CA, Ribon V, Kanzaki M, Thurmond DC, Mora S, Shigematsu S, Bickel PE, Pessin JE, Saltiel AR 2000 CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature 407:202-207
17. Gustavsson J, Parpal S, Karlsson M, Ramsing C, Thorn H, Borg M, Lindroth M, Peterson K H, Magnusson KE, StrâlforsP 1999 Localization of the insulin receptor in caveolae of adipocyte plasma membrane. FASEB J 13:1961-1971
18. Karlsson M, Thorn H, Parpal S, Strålfors P, Gustavsson J 2002 Insulin induces translocation of glucose transporter GLUT4 to plasma membrane caveolae in adipocytes. FASEB J 16:249-251
19. Parpal S, Karlsson M, Thorn H, Strålfors P 2001 Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J Biol Chem 276:9670-9678
20. Robinson LJ, Pang S, Harris DS, Heuser J, James DE 1992 Translocation of the glucose transporter (GLUT4) to the cell surface in permeabilized 3T3-L1 adipocytes: effects of ATP insulin, and GTPγS and localization of GLUT4 to clathrin lattices. J Cell Biol 117:1181-1196
21. Ros-Baro A, Lopez-Iglesias C, Peiro S, Bellido D, Palacin M, Zorzano A, Camps M 2001 Lipid rafts are required for GLUT4 internalization in adipose cells. Proc Natl Acad Sci USA 98:12050-12055
22. Shigematsu S, Watson RT, Khan AH, Pessin JE 2003 The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4. J Biol Chem 278:10683-10690
23. Blot V, McGraw TE 2006 GLUT4 is internalized by a cholesterol-dependent nystatin-sensitive mechanism inhibited by insulin. EMBO J 25:5648-5658
24. Watson RT, Shigematsu S, Chiang SH, Mora S, Kanzaki M, Macara IG, Saltiel AR, Pessin JE 2001 Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation. J Cell Biol 154:829-840
25. Chamberlain LH, Gould GW 2002 The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J Biol Chem 277:49750-49754
26. Muñoz P, Mora S, Sevilla L, Kaliman P, Tomàs E, Gumà A, Testar X, Palacín M, Zorzano A 1996 Expression and insulin-regulated distribution of caveolin in skeletal muscle. Caveolin does not colocalize with GLUT4 in intracellular membranes. J Biol Chem 271:8133-8139
27. Frost SC, Lane MD 1985 Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes. J Biol Chem 260:2646-2652
28. Naldini L, BlömerU, Gage FH, Trono D, Verma IM 1996 Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA 93:11382-11388
29. Brown DA, Rose JK 1992 Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544
30. Heuser JE, Anderson RG 1989 Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389-400
31. Reid G, HübnerMR, Metivier R, Brand H, Denger S, Manu D, Beaudouin J, Ellenberg J, Gannon F 2003 Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol Cell 11:695-707
32. Hansen JB, Petersen RK, Larsen BM, Bartkova J, Alsner J, Kristiansen K 1999 Activation of peroxisome proliferator-activated receptor γ bypasses the function of the retinoblastoma protein in adipocyte differentiation. J Biol Chem 274:2386-2393
33. Yang J, Clark AE, Kozka IJ, Cushman SW, Holman GD 1992 Development of an intracellular pool of glucose transporters in 3T3-L1 cells. J Biol Chem 267:10393-10399
34. Liu LB, Omata W, Kojima I, Shibata H 2007 The SUMO conjugating enzyme Ubc9 is a regulator of GLUT4 turnover and targeting to the insulin-responsive storage compartment in 3T3-L1 adipocytes. Diabetes 56:1977-1985
35. Biber JW, Lienhard GE 1986 Isolation of vesicles containing insulin-responsive, intracellular glucose transporters from 3T3-L1 adipocytes. J Biol Chem 261:16180-16184
36. Bach D, Naon D, Pich S, Soriano FX, Vega N, Rieusset J, Laville M, Guillet C, Boirie Y, Wallberg-Henriksson H, Manco M, Calvani M, Castagneto M, PalacínM, Mingrone G, Zierath JR, Vidal H, Zorzano A 2005 Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor α and interleukin-6. Diabetes 54:2685-2693
37. Sargiacomo M, Sudol M, Tang Z, Lisanti MP 1993 Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 122:789-807
38. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP 1996 Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 271:9690-9697
39. 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 2001 Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449-2452
40. Razani B, Lisanti MP 2001 Caveolin-deficient mice: insights into caveolar function human disease. J Clin Invest 108:1553-1561
41. Farese RV 2002 Function and dysfunction of αPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. Am J Physiol Endocrinol Metab 283:E1-E11
42. Welsh GI, Hers I, Berwick DC, Dell G, Wherlock M, Birkin R, Leney S, Tavaré JM 2005 Role of protein kinase B in insulin-regulated glucose uptake. Biochem Soc Trans 33:346-349
43. Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, Neudauer CL, Macara IG, Pessin JE, Saltiel AR 2001 Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410:944-948
44. Anderson RG 1998 The caveolae membrane system. Annu Rev Biochem 67: 199-225
45. Parton RG 1996 Caveolae and caveolins. Curr Opin Cell Biol 8:542-548
46. Ostrom RS, Liu X 2007 Detergent and detergent-free methods to define lipid rafts and caveolae. Methods Mol Biol 400:459-468
47. Ring A, Le Lay S, Pohl J, Verkade P, Stremmel W 2006 Caveolin-1 is required for fatty acid translocase (FAT/CD36) localization and function at the plasma membrane of mouse embryonic fibroblasts. Biochim Biophys Acta 1761:416-423
48. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B 2002 Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13:238-250
49. Ishiki M, Klip A 2005 Recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146:5071-5078
50. Krupp M, Lane MD 1981 On the mechanism of ligand-induced down-regulation of insulin receptor level in the liver cell. J Biol Chem 256:1689-1694
51. Green A, Olefsky JM 1982 Evidence for insulin-induced internalization and degradation of insulin receptors in rat adipocytes. Proc Natl Acad Sci USA 79:427-431
52. Ronnett GV, Knutson VP, Lane MD 1982 Insulin-induced down-regulation of insulin receptors in 3T3-L1 adipocytes. Altered rate of receptor inactivation. J Biol Chem 257:4285-4291
53. Heidenreich KA, Berhanu P, Brandenburg D, Olefsky JM 1983 Degradation of insulin receptors in rat adipocytes. Diabetes 32:1001-1009
54. Grako KA, Olefsky JM, McClain DA 1992 Tyrosine kinase-defective insulin receptors undergo decreased endocytosis but do not affect internalization of normal endogenous insulin receptors. Endocrinology 130:3441-3452
55. Yu ZW, Burén J, Enerbäck S, Nilsson E, Samuelsson L, Eriksson JW 2001 Insulin can enhance GLUT4 gene expression in 3T3-F442A cells and this effect is mimicked by vanadate but counteracted by cAMP and high glucose: potential implications for insulin resistance. Biochim Biophys Acta 1535: 174-185
56. Olson AL, Pessin JE 1995 Transcriptional regulation of the human GLUT4 gene promoter in diabetic transgenic mice. J Biol Chem 270:23491-23495
57. Olson AL, Liu ML, Moye-Rowley WS, Buse JB, Bell GI, Pessin JE 1993 Hormonal/metabolic regulation of the human GLUT4/muscle-fat facilitative glucose transporter gene in transgenic mice. J Biol Chem 268:9839-9846
58. Charron MJ, Katz EB, Olson AL 1999 GLUT4 gene regulation and manipulation. J Biol Chem 274:3253-3256
59. Gerrits PM, Olson AL, Pessin JE 1993 Regulation of the GLUT4/muscle-fat glucose transporter mRNA in adipose tissue of insulin-deficient diabetic rats. J Biol Chem 268:640-644
60. Hong S, Huo H, Xu J, Liao K 2004 Insulin-like growth factor-1 receptor signaling in 3T3-L1 adipocyte differentiation requires lipid rafts but not caveolae. Cell Death Differ 11:714-723
61. Yuan T, Hong S, Yao Y, Liao K 2007 Glut-4 is translocated to both caveolae and non-caveolar lipid rafts, but is partially internalized through caveolae in insulin-stimulated adipocytes. Cell Res 17:772-782
62. Kono T, Barham FW 1971 The relationship between the insulin-binding capacity of fat cells and the cellular response to insulin. Studies with intact and trypsin-treated fat cells. J Biol Chem 246:6210-6216
63. Kahn BB, Simpson IA, Cushman SW 1988 Divergent mechanisms for the insulin resistant and hyperresponsive glucose transport in adipose cells from fasted and refed rats. Alterations in both glucose transporter number and intrinsic activity. J Clin Invest 82:691-699
64. Powell KA, Campbell LC, Tavare JM, Leader DP, Wakefield JA, Gould GW 1999 Trafficking of Glut4-green fluorescent protein chimaeras in 3T3-L1 adipocytes suggests distinct internalization mechanisms regulating cell surface glut4 levels. Biochem J 344(Pt 2):535-543
65. Dugani CB, Klip A 2005 Glucose transporter 4: cycling, compartments and controversies. EMBO Rep 6:1137-1142