Free fatty acids inhibit insulin signaling-stimulated endothelial nitric oxide synthase activation through upregulating PTEN or inhibiting Akt kinase

Diabetes

Volumn 55, Issue 8, 2006, Pages 2301-2310

  Xing, Li Wang ^a   Zhang, Lin ^a   Youker, Keith ^a   Zhang, Ming Xiang ^a   Wang, Jian ^a   LeMaire, Scott A ^a   Coselli, Joseph S ^a   Shen, Ying H ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

ATF, activating transcription factor; CREBP, cAMP responsive element binding protein; EBM, endothelial cell basic medium; eNOS, endothelial nitric oxide synthase; FFA, free fatty acid; HAEC, human aortic endothelial cell

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; FATTY ACID; INSULIN; LINOLEIC ACID; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SYNAPTOPHYSIN; ATF2 PROTEIN, HUMAN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PALMITIC ACID; PROTEIN KINASE INHIBITOR; PTEN PROTEIN, HUMAN; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; INSULIN RELEASE; METABOLIC SYNDROME X; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM CELL; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 2; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FATTY ACIDS, NONESTERIFIED; HUMANS; INSULIN; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LINOLEIC ACID; NITRIC OXIDE SYNTHASE TYPE III; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PALMITIC ACID; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 33749329784     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db05-1574     Document Type: Article

References (50)

1. Kereiakes DJ, Willerson JT: Metabolic syndrome epidemic. Circulation 108:1552-1553, 2003
2. Haffner S, Taegtmeyer H: Epidemic obesity and the metabolic syndrome. Circulation 108:1541-1545, 2003
3. Aljada A, Dandona P: Effect of insulin on human aortic endothelial nitric oxide synthase. Metabolism 49:147-150, 2000
4. Zeng G, Nystrom FH, Ravichandran LV, Cong LN, Kirby M, Mostowski H, Quon MJ: Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101:1539-1545, 2000
5. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Targher G, Alberiche M, Bonadonna RC, Muggeo M: Prevalence of insulin resistance in metabolic disorders: the Bruneck Study. Diabetes 47:1643-1649, 1998
6. Laws A, Hoen HM, Selby JV, Saad MF, Haffner SM, Howard BV: Differences in insulin suppression of free fatty acid levels by gender and glucose tolerance status: relation to plasma triglyceride and apolipoprotein B concentrations: Insulin Resistance Atherosclerosis Study (IRAS) Investigators. Arterioscler Thromb Vasc Biol 17:64-71, 1997
7. Groop LC, Saloranta C, Shank M, Bonadonna RC, Ferrannini E, DeFronzo RA: The role of free fatty acid metabolism in the pathogenesis of insulin resistance in obesity and noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 72:96-107, 1991
8. Steinberg HO, Tarshoby M, Monestel R, Hook G, Cronin J, Johnson A, Bayazeed B, Baron AD: Elevated circulating free fatty acid levels impair endothelium-dependent vasodilation. J Clin Invest 100:1230-1239, 1997
9. Steinberg HO, Paradisi G, Hook G, Crowder K, Cronin J, Baron AD: Free fatty acid elevation impairs insulin-mediated vasodilation and nitric oxide production. Diabetes 49:1231-1238, 2000
10. Carlsson M, Wessman Y, Almgren P, Groop L: High levels of nonesterified fatty acids are associated with increased familial risk of cardiovascular disease. Arterioscler Thromb Vasc Biol 20:1588-1594, 2000
11. Jouven X, Charles MA, Desnos M, Ducimetiere P: Circulating nonesterified fatty acid level as a predictive risk factor for sudden death in the population. Circulation 104:756-761, 2001
12. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, Petersen KF, Shulman GI: Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest 103:253-259, 1999
13. Kuhlmann J, Neumann-Haefelin C, Belz U, Kalisch J, Juretschke HP, Stein M, Kleinschmidt E, Kramer W, Herling AW: Intramyocellular lipid and insulin resistance: a longitudinal in vivo 1H-spectroscopic study in Zucker diabetic fatty rats. Diabetes 52:138-144, 2003
14. Svedberg J, Bjorntorp P, Smith U, Lonnroth P: Free-fatty acid inhibition of insulin binding, degradation, and action in isolated rat hepatocytes. Diabetes 39:570-574, 1990
15. Shen YH, Zhang L, Gan Y, Wang X, Wang J, Lemaire SA, Coselli JS, Wang XL: Up-regulation of PTEN (phosphatase and tensin homolog deleted on chromosome ten) mediates p38 MAPK stress signal-induced inhibition of insulin signaling: a cross-talk between stress signaling and insulin signaling in resistin-treated human endothelial cells. J Biol Chem 281:7727-7736, 2006
16. Nicholson KM, Anderson NG: The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 14:381-395, 2002
17. Leslie NR, Downes CP: PTEN: the down side of PI 3-kinase signalling. Cell Signal 14:285-295, 2002
18. Vazquez F, Grossman SR, Takahashi Y, Rokas MV, Nakamura N, Sellers WR: Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J Biol Chem 276:48627-48630, 2001
19. Vazquez F, Ramaswamy S, Nakamura N, Sellers WR: Phosphorylation of the PTEN tail regulates protein stability and function. Mol Cell Biol 20:5010-5018, 2000
20. Manning AM, Davis RJ: Targeting JNK for therapeutic benefit: from junk to gold? Nat Rev Drug Discov 2:554-565, 2003
21. Koistinen HA, Chibalin AV, Zierath JR: Aberrant p38 mitogen-activated protein kinase signalling in skeletal muscle from type 2 diabetic patients. Diabetologia 46:1324-1328, 2003
22. Tan Y, Rouse J, Zhang A, Cariati S, Cohen P, Comb MJ: FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J 15:4629-4642, 1996
23. Hockings SC, Kahn JD, Crothers DM: Characterization of the ATF/CREB site and its complex with GCN4. Proc Natl Acad Sci U S A 95:1410-1415, 1998
24. Boden G: Effects of free fatty acids (FFA) on glucose metabolism: significance for insulin resistance and type 2 diabetes. Exp Clin Endocrinol Diabetes 111:121-124, 2003
25. Staiger H, Staiger K, Stefan N, Wahl HG, Machicao F, Kellerer M, Haring HU: Palmitate-induced interleukin-6 expression in human coronary artery endothelial cells. Diabetes 53:3209-3216, 2004
26. Tripathy D, Mohanty P, Dhindsa S, Syed T, Ghanim H, Aljada A, Dandona P: Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 52:2882-2887, 2003
27. Artwohl M, Roden M, Waldhausl W, Freudenthaler A, Baumgartner-Parzer SM: Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells. FASEB J 18:146-148, 2004
28. de Jongh RT, Serne EH, Ijzerman RG, de Vries G, Stehouwer CD: Free fatty acid levels modulate microvascular function: relevance for obesity-associated insulin resistance, hypertension, and microangiopathy. Diabetes 53:2873-2882, 2004
29. Egan BM, Lu G, Greene EL: Vascular effects of non-esterified fatty acids: implications for the cardiovascular risk factor cluster. Prostaglandins Leukot Essent Fatty Acids 60:411-420, 1999
30. Kim F, Tysseling KA, Rice J, Pham M, Haji L, Gallis BM, Baas AS, Paramsothy P, Giachelli CM, Corson MA, Raines EW: Free fatty acid impairment of nitric oxide production in endothelial cells is mediated by IKKbeta. Arterioscler Thromb Vasc Biol 25:989-994, 2005
31. Baron AD: Vascular reactivity. Am J Cardiol 84:25J-27J, 1999
32. Gratton JP, Fontana J, O'Connor DS, Garcia-Cardena G, McCabe TJ, Sessa WC: Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro: evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J Biol Chem 275:22268-22272, 2000
33. Takahashi S, Mendelsohn ME: Synergistic activation of endothelial nitric-oxide synthase (eNOS) by HSP90 and Akt: calcium-independent eNOS activation involves formation of an HSP90-Akt-CaM-bound eNOS complex. J Biol Chem 278:30821-30827, 2003
34. Wyatt AW, Steinert JR, Wheeler-Jones CP, Morgan AJ, Sugden D, Pearson JD, Sobrevia L, Mann GE: Early activation of the p42/p44MAPK pathway mediates adenosine-induced nitric oxide production in human endothelial cells: a novel calcium-insensitive mechanism. FASEB J 16:1584-1594, 2002
35. Morrow VA, Foufelle F, Connell JM, Petrie JR, Gould GW, Salt IP: Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J Biol Chem 278:31629-31639, 2003
36. Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S: Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab 86:3257-3265, 2001
37. Aljada A, Ghanim H, Assian E, Dandona P: Tumor necrosis factor-alpha inhibits insulin-induced increase in endothelial nitric oxide synthase and reduces insulin receptor content and phosphorylation in human aortic endothelial cells. Metabolism 51:487-491, 2002
38. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M: IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11:191-198, 2005
39. Cai D, Yuan M, Frantz DF, Melendez PA, Hansen L, Lee J, Shoelson SE: Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 11:183-190, 2005
40. Jiang G, Zhang BB: Pi 3-kinase and its up- and down-stream modulators as potential targets for the treatment of type II diabetes. Front Biosci 7:d903-d907, 2002
41. Stiles B, Wang Y, Stahl A, Bassilian S, Lee WP, Kim YJ, Sherwin R, Devaskar S, Lesche R, Magnuson MA, Wu H: Live-specific deletion of negative regulator Pten results in fatty liver and insulin hypersensitivity. Proc Natl Acad Sci U S A 101:2082-2087, 2004
42. Wijesekara N, Konrad D, Eweida M, Jefferies C, Liadis N, Giacca A, Crackower M, Suzuki A, Mak TW, Kahn CR, Klip A, Woo M: Muscle-specific Pten deletion protects against insulin resistance and diabetes. Mol Cell Biol 25:1135-1145, 2005
43. Kurlawalla-Martinez C, Stiles B, Wang Y, Devaskar SU, Kahn BB, Wu H: Insulin hypersensitivity and resistance to streptozotocin-induced diabetes in mice lacking PTEN in adipose tissue. Mol Cell Biol 25:2498-2510, 2005
44. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM: Enhanced basal activation of mitogen-activated protein kinases in adipocytes from type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression. Diabetes 52:634-641, 2003
45. De Alvaro C, Teruel T, Hernandez R, Lorenzo M: Tumor necrosis factor-alpha produces insulin resistance in skeletal muscle by activation of inhibitor kB kinase in a p38 mitogen-activated protein kinase-dependent manner. J Biol Chem 279:17070-17078, 2004
46. Huang C, Somwar R, Patel N, Niu W, Torok D, Klip A: Sustained exposure of L6 myotubes to high glucose and insulin decreases insulin-stimulated GLUT4 translocation but upregulates GLUT4 activity. Diabetes 51:2090-2098, 2002
47. Aguirre V, Uchida T, Yenush L, Davis R, White MF: The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275:9047-9054, 2000
48. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS: A central role for JNK in obesity and insulin resistance. Nature 420:333-336, 2002
49. Lee YH, Giraud J, Davis RJ, White MF: c-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade. J Biol Chem 278:2896-2902, 2003
50. De Fea K, Roth RA: Modulation of insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. J Biol Chem 272:31400-31406, 1997