Effect of cholesterol depletion on mitogenesis and survival: The role of caveolar and noncaveolar domains in insulin-like growth factor-mediated cellular function

Endocrinology

Volumn 146, Issue 12, 2005, Pages 5463-5473

  Matthews, Laura C ^a   Taggart, Michael J ^a   Westwood, Melissa ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; CHOLESTEROL; CYCLODEXTRIN DERIVATIVE; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SOMATOMEDIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL FUNCTION; CELL MEMBRANE; CELL PROLIFERATION; CELL STRAIN 3T3; CELL STRAIN HEPG2; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIPID RAFT; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STATISTICAL SIGNIFICANCE; SURVIVAL;

ANIMALS; BETA-CYCLODEXTRINS; CAVEOLAE; CAVEOLINS; CELL LINE; CELL PHYSIOLOGY; CELL SURVIVAL; CELLS; CHOLESTEROL; HUMANS; MICE; MITOSIS; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; SOMATOMEDINS; TISSUE DISTRIBUTION;

EID: 27844583380     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0236     Document Type: Article

References (48)

1. 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
2. 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 in adipose tissue. Am J Physiol 285:C222-C235
3. Oshikawa J, Otsu K, Toya Y, Tsunematsu T, Hankins R, Kawabe JI, Minamisawa S, Umemura S, Hagiwara Y, Ishikawa Y 2004 Insulin resistance in skeletal muscles of caveolin-3-null mice. Proc Natl Acad Sci USA 101:12670-12675
4. Park D, Cohen AW, Frank PG, Razani B, Lee H, Williams TM, Chandra M, Shirani J, De Souza AP, Tang B, Jelicks LA, Factor SM, Weiss LM, Tanowitz HB, Lisanti MP 2003 Caveolin-1 null mice show dramatic reductions in life span. Biochemistry 42:15124-15131
5. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP 2001 Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276:38121-38138
6. Park DS, Woodman SE, Schubert AL, Cohen AW, Frank PG, Chandra M, Shirani J, Razani B, Tang B, Jelicks LA, Factor SM, Weiss LM, Tanowitz HB, Lisanti MP 2002 Caveolin-1/3 double-knockout mice are viable, but lack both muscle and non-muscle caveolae, and develop a severe cardiomyopathic phenotype. Am J Pathol 160:2207-2217
7. Mineo C, James GL, Smart EJ, AndersonRGW1996 Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J Biol Chem 271:11930-11935
8. Yamamoto M, Toya Y, Jensen RA, Ishikawa Y 1999 Caveolin is an inhibitor of platelet-derived growth factor receptor signaling. Exp Cell Res 247:380-388
9. Li S, Couet J, Lisanti MP 1996 Src tyrosine kinases, Gα subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. J Biol Chem 271:29182-29190
10. Chun M, Liyanage U, Lisanti MP, Lodish HF 1994 Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc Natl Acad Sci USA 91:11728-11732
11. Schlegel A, Wang C, Pestell RG, Lisanti MP 2001 Ligand-independent activation of oestrogen receptor α by caveolin-1. Biochem J 359:203-210
12. Gustavsson J, Parpal S, Karlsson M, Ramsing C, Thorn H, Borg M, Lindroth M, Peterson KH, Magnusson KE, Stralfors P 1999 Localization of the insulin receptor in caveolae of adipocyte plasma membrane. FASEB J 13:1961-1971
13. Parpal S, Karlsson M, Thorn H, Stralfors P 2001 Cholesterol depletion disrupts caveolae and insulin receptor signalling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J Biol Chem 276:9670-9678
14. Yamamoto M, Toya Y, Schwenke C, Lisanti MP, Myers MG, Ishikawa Y 1998 Caveolin is an activator of insulin receptor signaling. J Biol Chem 273:26962-26968
15. Coppola D, Ferber A, Miura M, Sell C, D'Ambrosio C, Rubin R, Baserga R 1994 A functional insulin-like growth factor I receptor is required for the mitogenic and transforming activities of the epidermal growth factor receptor. Mol Cell Biol 14:4588-4595
16. Benito M, Valverde AM, Lorenzo M 1996 IGF-I: a mitogen also involved in differentiation processes in mammalian cells. Int J Cell Biol 28:499-510
17. Leventhal PS, Feldman EL 1997 Insulin-like growth factors as regulators of cell motility. Trends Endocrinol Metab 8:1-6
18. Baudry A, Lamothe B, Bucchini D, Jami J, Montarras D, Pinset C, Joshi RL 2001 IGF-I receptor as an alternative receptor for metabolic signaling in insulin receptor-deficient muscle cells. FEBS Lett 488:174-178
19. O'Connor R, Kauffmann-Zeh A, Liu Y, Lehar S, Evan GI, Baserga R, Blattler WA 1997 Identification of domains of the insulin-like growth factor I receptor that are required for protection from apoptosis. Mol Cell Biol 17:427-436
20. Huo H, Guo X, Hong S, Jiang M, Liu X, Liao K 2003 Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction. J Biol Chem 278:11561-11569
21. Hong S, Huo H, Xu J, Liao K 2004 Insulin-like growth factor-1 receptor signalling in 3T3-l1 adipocyte differentiation requires lipid rafts but not caveolae. Cell Death Differ 11:714-723
22. Christian AE, Haynes MP, Phillips MC, Rothblat GH 1997 Use of cyclodextrins for manipulating cellular cholesterol content. J Lipid Res 38:2264-2272
23. Hailstones D, Sleer LS, Parton RG, Stanley KK 1998 Regulation of caveolin and caveolae by cholesterol in MDCK cells. J Lipid Res 39:369-379
24. Blakesely VA, Kato H, Roberts CT, LeRoith D 1995 Mutation of a conserved amino acid residue (tryptophan 1171) in the tyrosine kinase domain of the IGF-I receptor abolishes autophosphorylation but does not eliminate biologic function. J Biol Chem 270:2764-2769
25. Smart EJ, Ying Y, Mineo C, AndersonRGW1995 A detergent-free method for purifying caveoolae membrane from tissue culture cells. Proc Natl Acad Sci USA 92:10104-10108
26. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K 1995 VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92:10339-10343
27. Podar K, Tai YT, Cole CE, Hideshima T, Sattler M, Hamblin A, Mitsiades N, Schlossman RL, Davies FE, Morgan GJ, Munshi NC, Chauhan D, Anderson KC 2003 Essential role of caveolae in IL-6- and IGF-I-triggered Akt-1-mediated survival of multiple myeloma cells. J Biol Chem 278:5794-5801
28. 473 phosphorylation by protein kinase Cα in endothelial cells. Cell Signal 16:951-957
29. Cohen AW, Combs TP, Scherer PE, Lisanti MP 2003 Role of caveolin and caveolin in insulin signaling and diabetes. Am J Physiol Endocrinol Metab 285:E1151-E1160
30. Peres C, Yart A, Perret B, Salles JP, Raynal P 2003 Modulation of phosphoinositide 3-kinase activation by cholesterol level suggests a novel positive role for lipid rafts in lysophosphatidic acid signalling. FEBS Lett 534:164-168
31. Halevy O, Cantley LC 2004 Differential regulation of the phosphoinositide 3-kinase and MAP kinase pathways by hepatocyte growth factor vs. insulinlike growth factor-I in myogenic cells. Exp Cell Res 297:224-234
32. Radcliff K, Tang TB, Lim J, Zhang Z, Abedin M, Demer, LL, Tintut Y 2005 Insulin-like growth factor-I regulates proliferation and osteoblastic differentiation of calcifying vascular cells via extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase pathways. Circ Res 96:398-400
33. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M 2002 Regulation of Raf-Akt crosstalk. J Biol Chem 277:31099-31106
34. Zhuang L, Lin J, Lu ML, Solomon KR, Freeman MR 2002 Cholesterol-rich lipid rafts mediate akt-regulated survival in prostate cancer cells. Cancer Res 62:2227-2231
35. Furuchi T, Anderson RGW 1998 Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-regulated kinase (ERK). J Biol Chem 273:21099-21104
36. Hua H, Munk S, Whiteside CI 2003 Endothelin-1 activates mesangial cell ERK1/2 via EGF-receptor transactivation and caveolin-1 interaction. Am J Physiol Renal Physiol 284:F303-F312
37. Karlsson M, Thorn H, Danielsson A, Stenkula KG, Ost A, Gustavsson J, Nystrom FH, Stralfors P 2004 Colocalisation of insulin receptor and insulin receptor substrate-1 to caveolae in primary human adipocytes. Cholesterol depletion blocks insulin signalling for metabolic and mitogenic control. Eur J Biochem 271:2471-2479
38. Nystrom F, Chen H, Cong L, 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
39. Zimmermann S, Moelling K 1999 Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286:1741-1744
40. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ 1999 Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741
41. Panetta D, Biedi C, Repetto S, Cordera R, Maggi D 2004 IGF-I regulates caveolin 1 and IRS-1 interaction in caveolae. Biochem Biophys Res Commun 316:240-243
42. Ushio-Fukai M, Hilenski L, Santanam N, Becker PL, Ma X, Griendling KK, Alexander RW 2001 Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells. J Biol Chem 276:48269-48275
43. Pietrzkowski Z, Sell C, Lammers R, Ullrich A, Baserga R 1992 Roles of insulinlike growth factor 1 (IGF-1) and the IGF-1 receptor in epidermal growth factor-stimulated growth of 3T3 cells. Mol Cell Biol 12:3883-3889
44. Gilmore AP, Valentijn AJ, Wang P, Ranger AM, Bundred N, O'Hare MJ, Wakeling A, Korsmeyer SJ, StreuliCH2002 Activation of BAD by therapeutic inhibition of epidermal growth factor receptor and transactivation by insulinlike growth factor receptor. J Biol Chem 277:27643-27650
45. Zahradka P, Litchie B, Storie B, Helwer G 2004 Transactivation of the insulinlike growth factor-I receptor by angiotensin II mediates downstream signaling from the angiotensin II type 1 receptor to phosphatidylinositol 3-kinase. Endocrinology 145:2978-2987
46. Roudabush FL, Pierce KL, Maudsley S, Khan KD, Luttrell LM 2000 Transactivation of the EGF receptor mediates IGF-I-stimulated Shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem 275:22583-22589
47. Di Fiore P, GillGN 1999 Endocytosis and mitogenic signaling. Curr Opin Cell Biol 11:483-488
48. Pol A, Lu A, Pons M, Peiro S, Enrich K 2000 Epidermal growth factormediated caveolin recruitment to early endosomes andMAPKactivation. J Biol Chem 275:30566-30572