Rescuing 3T3-L1 adipocytes from insulin resistance induced by stimulation of akt-mammalian target of rapamycin/p70 S6 kinase (S6K1) pathway and serine phosphorylation of insulin receptor substrate-1: Effect of reduced expression of p85α subunit of phosphatidylinositol 3-kinase and S6K1 kinase

Endocrinology

Volumn 150, Issue 3, 2009, Pages 1165-1173

  Adochio, Rebecca ^a,b   Leitner, J Wayne ^a   Hedlund, Reed ^a   Draznin, Boris ^a,b,c,d  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c Adult Diabetes Program

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 1; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85; PROTEIN P85ALPHA; S6 KINASE; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN KINASE; PROTEIN SUBUNIT; RPS6KA1 PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; ENZYME SUBUNIT; FEEDBACK SYSTEM; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; GLUCOSE TRANSPORT; HORMONE ACTION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; EVALUATION STUDY; GENE THERAPY; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROCEDURES; PROTEIN SUBUNIT;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; GENETIC THERAPY; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MICE; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN SUBUNITS; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA, SMALL INTERFERING; SERINE; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFECTION;

EID: 67649854830     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0437     Document Type: Article

References (69)

1. Qiao L, Goldberg JL, Russell JC, Sun XJ 1999 Identification of enhanced serine kinase activity in insulin resistance. J Biol Chem 274:10625-10632
2. White MF 2003 Insulin signaling in health and disease. Science 302:1710-1711
3. Birnbaum MJ 2001 Turning down insulin signaling. J Clin Invest 108:655-659
4. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF 2002 Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277:1531-1537
5. Shah OJ, Wang Z, Hunter T 2004 Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr Biol 14:1650-1656
6. Khamzina L, Veilleux A, Bergeron S, Marette A 2005 Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146:1473-1481
7. Trembley F, Gagnon A, Veilleux A, Sorisky A, Marette A 2005 Activation of the mammalian target of rapamycin pathway acutely inhibits insulin signaling to Akt and glucose transport in 3T3-L1 and human adipocytes. Endocrinology 146:1328-337
8. Draznin B 2006 Molecular mechanisms of insulin resistance: serine phosphorylation of insulin receptor substrate-1 and increased expression of p85α. Diabetes 55:2392-2397
9. Shepherd PR, Withers DJ, Siddle K 1998 Phosphoinositide 3-kinase: the key switch mechanism in insulin signaling. Biochem J 333:471-490
10. Terauchi Y, Tsuji Y, Satoh S, Minoura H, Murakami K, Okuno A, Inukai K, Asano T, Kaburagi Y, Ueki K, Nakajima H, Hanafusa T, Matsuzawa Y, Sekihara H, Yin Y, Barrett JC, Oda H, Ishikawa T, Akanuma Y, Komuro I, Suzuki M, Yamamura K-I, Kodama T, Suzuki H, Koyasu S, Aizawa S, Tobe K, Fukui Y, Yazaki Y, Kadowaki T 1999 Increased insulin sensitivity and hypoglycaemia in mice lacking the p85α subunit of phosphoinositide 3-kinase. Nat Genet 21:230-235
11. Ueki K, Algenstaedt P, Mauvais-Jarvis F, Kahn CR 2000 Positive and negative regulation of phosphoinositide 3-kinase-dependent signaling pathways by three different gene products of the p85a regulatory subunit. Mol Cell Biol 20:8035-8046
12. Mauvais-Jarvis F, Ueki K, Fruman DA, Hirshman MF, Sakamoto K, Goodyear LJ, Iannacone M, Accili D, Cantley LC, Kahn CR 2002 Reduced expression of the murine p85α subunit of phosphoinositide 3-kinase improves insulin signaling and ameliorates diabetes. J Clin Invest 109:141-149
13. Ueki K, Fruman DA, Uballe CM, Fasshauer M, Klein J, Asano T, Cantley LC, Kahn CR 2003 Positive and negative roles of p85α and p85β regulatory sub-units of phosphoinositide 3-kinase in insulin signaling. J Biol Chem 278:48453-48466
14. Barbour L, Rahman SM, Gurevich I, Leitner JW, Fisher S, Roper M, Knotts T, Vo Y, Yakar S, LeRoith D, Kahn CR, Cantley L, Friedman J, Draznin B 2005 Increased p85α is a potent negative regulator of skeletal muscle insulin signaling and induces in vivo insulin resistance associated with growth hormone excess. J Biol Chem 280:37489-37494
15. Del Rincon JP, Iida K, Gaylinn BD, McCurdy CE, Leitner JW, Barbour LA, Kopchick JJ, Friedman JE, Draznin B, Thorner MO 2007 Growth hormone regulation of p85α expression and phosphoinositide 3-kinase activity in adipose tissue. Diabetes 56:1638-1646
16. Raught B, Gingras AC, Sonenberg N 2001 The target of rapamycin (TOR) proteins. Proc Natl Acad Sci USA 98:7037-7044
17. Rohde J, Heitman J, Cardenas ME 2001 The TOR kinases link nutrient sensing to cell growth. J Biol Chem 276:9583-9586
18. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM 1998 RAFT phosphorylation of the translational regulators p70S6 kinase and 4E-BP1. Proc Natl Acad Sci USA 95:1432-1437
19. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng OP, Kasuga M, Nishimoto I, Avruch J 1997 Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem 272:26457-26463
20. Isotani S, Hara K, Tokunaga C, Inoue H, Avruch J, Yonezawa K 1999 Immunopurified mammalian target of rapamycin phosphorylates and activates p70S6 kinase α in vitro. J Biol Chem 274:34493-34498
21. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR 1999 Mammalian target of rapamycin is a direct target for protein kinase B: Identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344:427-431
22. Scott PH, Brunn GJ, Kohn AD, Roth RA, Lawrence Jr JC 1998 Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. Proc Natl Acad Sci USA 95:7772-7777
23. Hinault C, Mothe-Satney I, Gautier N, Lawrence Jr JC, Van Obberghen E 2004 Amino acids and leucine allow insulin activation of the PKB/mTOR pathway in normal adipocytes treated with wortmannin and in adipocytes from db/db mice. FASEB J 18:1894-1896
24. Pham PT, Heydrick SJ, Fox HL, Kimball SR, Jefferson Jr LS, Lynch CJ 2000 Assessment of cell-signaling pathways in the regulation of mammalian target of rapamycin (mTOR) by amino acids in rat adipocytes. J Cell Biochem 79:427-441
25. Cheatham B, Kahn CR 1995 Insulin action and the insulin signaling network. Endocr Rev 16:117-141
26. Pende M, Kozma SC, Jaquet M, Oorschot V, Burcelin R, Le Marchand-Brustel Y, Klumperman J, Thorens B, Thomas G 2000 Hypoinsulinemia, glucose intolerance and diminished β-cell size in S6K1-deficient mice. Nature 408:994-997
27. Tremblay F, Krebs M, Dombrowski L, Brehm A, Bernroider E, Roth E, Nowotny P, Waldhausl W, Marette A, Roden M 2005 Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54:2674-2684
28. Ueno M, Carvalheira J Biol Chem, Tambascia RC, Bezerra RMN, Amaral ME, Carniero EM, Folli F, Franchini KG, Saad MJA 2005 Regulation of insulin signaling by hyperinsulinemia: role of IRS-1/2 serine phosphorylation and mTOR/p70 S6K pathway. Diabetologia 48:506-518
29. Matsushima R, Harada N, Webster NJ, Tsutsumi YM, Nakaya Y 2006 Effect of TRB3 on insulin and nutrient-stimulated hepatic p70 S6 kinase activity. J Biol Chem 281:29719-29729
30. Shima H, Pende M, Chen Y, Fumagalli S, Thomas G, Kozma SC 1998 Disruption of the p70s6k/p85s6k gene reveals asmall mouse phenotype and a new functional S6 kinase. EMBO J 17:6649-6659
31. Um SH, Frigerio F, Watanabe M, Picard F, Jaoquin M, Sticker M, Fumagalli S, Allegrin PR, Kozma SC, Auwerx J, Thomas G 2004 Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431:200-205
32. Kohn AD, Summers SA, Birnbaum MJ, Roth RA 1996 Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem 271:31372-31378
33. Kahn BB, Flier JS 2000 Obesity and insulin resistance. J Clin Invest 106:473-481
34. Pessin JE, Saltiel AR 2000 Signaling pathways in insulin action: molecular targets of insulin resistance. J Clin Invest 106:165-169
35. LeRoith D, Zick Y 2001 Recent advances in our understanding of insulin action and insulin resistance. Diabetes Care 24:588-597
36. Qiao L, Zhande R, Jetton TL, Zhou G, Sun XJ 2002 In vivo phosphorylation of insulin receptor substrate 1 atserine 789 bya novel serine kinase in insulin-resistant rodents. J Biol Chem 277:26530-26539
37. Hirosumi J, Tuncman G, Chang L, Gorzun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS 2002 A central role for JNK in obesity and insulin resistance. Nature 420:333-336
38. Gao Z, Zhang X, Zuberi A, Hwang D, Quon MJ, Lefevre M, Ye J 2004 Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes. Mol Endocrinol 18:2024-2034
39. Nguyen MT, Satoh H, Favelyukis S, Babendure JL, Imamura T, Sbodio JI, Zalevsky J, Dahiyat B, Chi NW, Olefsky JM 2005 JNK and tumor necrosis factor-α mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J Biol Chem 282:35361-35371
40. Bandyopadhyay GK, Yu JG, Ofrecio J, Olefsky JM 2005 Increased p85/55/50 expression and decreased phosphatidylinositol 3-kinase activity in insulin-resistant human skeletal muscle. Diabetes 54:2351-2359
41. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M, Shoelson SE 2001 Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of IKK-β. Science 293:1673-1677
42. Perseghin G, Petersen K, Shulman GI 2003 Cellular mechanism of insulin resistance: potential links with inflammation. Int J Obes Relat Metab Disord 27(Suppl 3):S6-S11
43. Gao Z, Hwang D, Bataille F, Lefevre, York D, Quon MJ, Ye J 2002 Serine phosphorylation of insulin receptor substrate 1 by inhibitor kB kinase complex. J Biol Chem 277:48115-48121
44. Kim JK, Kim YJ, Fillmore JJ, Chen Y, Moore I, Lee J, Yuan M, Li ZW, Karin M, Perret P, Shoelson SE, Shulman GI 2001 Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 108:437-446
45. Hundal RS, Petersen KF, Mayerson AB, Rahdhawa PS, Inzucchi S, Shoelson SE, Shulman GI 2002 Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J Clin Invest 109:1321-1326
46. Hotamisligil GS, Spiegelman BM 1994 Tumor necrosis factor α: a key component of the obesity-diabetes link. Diabetes 43:1271-1278
47. Qi C, Pekala PH 2000 Tumor necrosis factor-α-induced insulin resistance in adipocytes. Proc Soc Exp Biol Med 223:128-135
48. Hotamisligil GS, Shargill NS, Spiegelman BM 1993 Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science 259:87-91
49. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS 1997 Protection from obesity-induced insulin resistance in mice lacking TNF-α function. Nature 389:610-614
50. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM 1996 IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-α and obesity-induced insulin resistance. Science 271:665-668
51. Lowell BB, Shulman GI 2005 Mitochondrial dysfunction and type 2 diabetes. Science 307:384-387
52. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI 2003 Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300:1140-1142
53. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI 2004 Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664-671
54. Li Y, Soos TJ, Li X, Wu J, Degennaro M, Sun X, Littman DR, Birnbaum MJ, Polakiewicz RD 2004 Protein kinase θ inhibits insulin signaling by phosphorylating IRS1 at Ser1101. J Biol Chem 279:45304-45307
55. Bell KS, Shcmitz-Peiffer C, Lim-Fraser M, Biden TJ, Cooney GJ, Kraegen EW 2000 Acute reversal of lipid-induced muscle insulin resistance is associated with rapid alteration in PKC-θ localization. Am J Physiol Endocrinol Metab 279:E1196-E1201
56. Kim JK, Fillmore JJ, Sunshine MJ, Albrecht B, Higashimori T, Kim DW, Liu ZX, Soos TJ, Cline GW, O'Brien WR, Littman DR, Shulman GI 2004 PKC-θ knockout mice are protected from fat-induced insulin resistance. J Clin Invest 114:823-827
57. Itani SI, Pories WJ, Macdonald KG, Dohm GL 2001 Increased protein kinase C θ in skeletal muscle of diabetic patients. Metabolism 50:553-557
58. Haruta T, Uno T, Kawahara J, Takano A, Egawa K, Sharma PM, Olefsky JM, Kobayashi M 2000 A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol 14:783-794
59. Tremblay F, Marette A 2001 Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle. J Biol Chem 276:38052-38060
60. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H, Barnett J, Leslie NR, Cheng S, Shepherd PR, Gout I, Downes CP, Lamb RE 2004 The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J Cell Biol 166:213-223
61. Lee YH, Giraud J, Davis RJ, White MF 2003 C-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade. J Biol Chem 278:2896-2902
62. Dann SG, Selvaraj A, Thomas G 2007 mTOR complex-1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol Med 13:252-259
63. Ueki K, Fruman DA, Brachmann SM, Tseng YH, Cantley LC, Kahn CR 2002 Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival. Mol Cell Biol 22:965-977
64. Barbour LA, Shao J, Qiao L, Leitner W, Anderson M, Friedman JE, Draznin B 2004 Human placental growth hormone increases expression of p85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle. Endocrinology 145:1144-1150
65. Cornier MA, Bessesen DH, Gurevich I, Leitner JW, Draznin B 2006 Nutritional up-regulation of p85α expression is an early molecular manifestation of insulin resistance. Diabetologia 49:748-754
66. Ueki K, Yballe CM, Brachmann SM, Vicent D, Watt JM, Kahn CR, Cantley LC 2002 Increased insulin sensitivity in mice lacking p85β subunit of phosphoinositide 3-kinase. Proc Natl Acad Sci USA 99:419-424
67. Lamia KA, Peroni OD, Kim Y-B, Rameh LE, Kahn BB, Cantley LC 2004 Increased insulin sensitivity and reduced adiposity in phosphatidylinositol 5-phosphate 4-kinase β-/- mice. Mol Cell Biol 24:5080-5087
68. Luo J, Field SJ, Lee JY, Engelman JA, Cantley LC 2005 The p85 regulatory subunit of phosphoinositide 3-kinase down-regulates IRS-1 signaling via the formation of a sequestration complex. J Cell Biol 170:455-464
69. Kirwan J, Varastehpour A, Jing M, Presley L, Shao J, Friedman JE, PM Catalano 2004 Reversal of insulin resistance post-partum is linked to enhanced skeletal muscle insulin signaling. J Clin Endocrinol Metab 89:4678-4684