Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 25, Issue 6, 2005, Pages 1142-1147

  Taniyama, Yoshihiro ^a   Hitomi, Hirofumi ^a   Shah, Anand ^a   Alexander, R Wayne ^a   Griendling, Kathy K ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin II; Insulin; Insulin resistance; IRS 1; Phosphoinositide dependent kinase 1; Vascular smooth muscle

Indexed keywords

ACETYLCYSTEINE; ANGIOTENSIN; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIOXIDANT; CATALASE; EBSELEN; GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; PHOSPHATIDYLINOSITOL KINASE; PHOSPHATIDYLINOSITOL KINASE 1; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; SERINE; UNCLASSIFIED DRUG; VALSARTAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GLUCOSE TRANSPORT; IMMUNOPRECIPITATION; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

ANGIOTENSIN II; ANIMALS; AORTA, THORACIC; CELLS, CULTURED; DOWN-REGULATION; HYPOGLYCEMIC AGENTS; INSULIN; MUSCLE, SMOOTH, VASCULAR; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; REACTIVE OXYGEN SPECIES; SERINE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; VASOCONSTRICTOR AGENTS;

EID: 20144367205     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000164313.17167.df     Document Type: Article

References (43)

1. Kim YK, Lee MS, Son SM, Kim IJ, Lee WS, Rhim BY, Hong KW, Kim CD. Vascular NADH oxidase is involved in impaired endothelium-dependent vasodilation in OLETF rats, a model of type 2 diabetes. Diabetes. 2002;51:522-527.
2. Schofield I, Malik R, Izzard A, Austin C, Heagerty A. Vascular structural and functional changes in type 2 diabetes mellitus: evidence for the roles of abnormal myogenic responsiveness and dyslipidemia. Circulation. 2002;106:3037-3043.
3. Tooke JE. Possible pathophysiological mechanisms for diabetic angiopathy in type 2 diabetes. J Diabetes Complications. 2000;14:197-200.
4. Igarashi M, Hirata A, Yamaguchi H, Tsuchiya H, Ohnuma H, Tominaga M, Daimon M, Kato T. Candesartan inhibits carotid intimal thickening and ameliorates insulin resistance in balloon-injured diabetic rats. Hypertension. 2001;38:1255-1259.
5. Elhadd TA, Kennedy G, Hill A, McLaren M, Newton RW, Greene SA, Belch JJ. Abnormal markers of endothelial cell activation and oxidative stress in children, adolescents and young adults with type 1 diabetes with no clinical vascular disease. Diabetes Metab Res Rev. 1999;15:405-411.
6. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, Channon KM. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation. 2002;105:1656-1662.
7. Egan BM, Greene EL, Goodfriend TL. Insulin resistance and cardiovascular disease. Am J Hypertens. 2001;14:116S-125S.
8. Henriksen EJ, Jacob S, Kinnick TR, Teachey MK, Krekler M. Selective angiotensin II receptor antagonism reduces insulin resistance in obese Zucker rats. Hypertension. 2001;38:884-890.
9. O'Driscoll G, Green D, Maiorana A, Stanton K, Colreavy F, Taylor R. Improvement in endothelial function by angiotensin-converting enzyme inhibition in non-insulin-dependent diabetes mellitus. J Am Coll Cardiol. 1999;33:1506-1511.
10. Reddi AS, Nimmagadda VR, Arora R. Effect of antihypertensive therapy on renal artery structure in type 2 diabetic rats with hypertension. Hypertension. 2001;37:1273-1278.
11. Sykiotis GP, Papavassiliou AG. Serine phosphorylation of insulin receptor substrate-1: a novel target for the reversal of insulin resistance. Mol Endocrinol. 2001;15:1864-1869.
12. Yenush L, White MF. The IRS-signaling system during insulin and cytokine action. BioEssays. 1997;19:491-500.
13. De Fea K, Roth RA. Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612. Biochemistry. 1997;36:12939-12947.
14. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem. 2002;77:1531-1537.
15. Pederson TM, Kramer DL, Rondinone CM. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes. 2001;50:24-31.
16. Greene MW, Sakaue H, Wang L, Alessi DR, Roth RA. Modulation of insulin-stimulated degradation of human insulin receptor substrate-1 by Serine 312 phosphorylation. J Biol Chem. 2003;278:8199-8211.
17. Rui L, Aguirre V, Kim JK, Shulman GI, Lee A, Corbould A, Dunaif A, White MF. Insulin/IGF-1 and TNF-alpha stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways. J Clin Invest. 2001;107:181-189.
18. Gao Z, Hwang D, Bataille F, Lefevre M, York D, Quon MJ, Ye J. Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J Biol Chem. 2002;277:48115-48121.
19. Haruta T, Uno T, Kawahara J, Takano A, Egawa K, Sharma PM, Olefsky JM, Kobayashi M. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol. 2000;14:783-794.
20. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148.
21. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP. Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J Clin Invest. 1997;100:2158-2169.
22. Motley ED, Eguchi K, Gardner C, Hicks AL, Reynolds CM, Frank GD, Mifune M, Ohba M, Eguchi S. Insulin-induced Akt activation is inhibited by angiotensin II in the vasculature through protein kinase C-alpha. Hypertension. 2003;41:775-780.
23. Taniyama Y, Weber DS, Rocic P, Hilenski L, Akers ML, Park J, Hemmings BA, Alexander RW, Griendling KK. Pyk2- and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol Cell Biol. 2003;23:8019-8029.
24. Griendling KK, Taubman MB, Akers M, Mendlowitz M, Alexander RW. Characterization of phosphatidylinositol-specific phospholipase C from cultured vascular smooth muscle cells. J Biol Chem. 1991;266:15498-15504.
25. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, Taylor WR, Griendling KK. Novel role of NADH/NADPH oxidase-derived hydrogen peroxide in angiotensin II-induced hypertrophy of rat vascular smooth muscle cells. Hypertension. 1998;32:488-495.
26. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem. 1999;274:22699-22704.
27. Griendling KK, Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept. 2000;91:21-27.
28. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res. 2002;91:406-413.
29. Ishida M, Marrero MB, Schieffer B, Ishida T, Bernstein KE, Berk BC. Angiotensin II activates pp60c-src in vascular smooth muscle cells. Circ Res. 1995;77:1053-1059.
30. Zhande R, Mitchell JJ, Wu J, Sun XJ. Molecular mechanism of insulin-induced degradation of insulin receptor substrate 1. Mol Cell Biol. 2002;22:1016-1026.
31. Heart Outcomes Prevention Evaluation Study Investigators. Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy. Lancet. 2000;355:253-259.
32. Julius S, Kjeldsen SE, Weber M, Brunner HR, Ekman S, Hansson L, Hua T, Laragh J, McInnes GT, Mitchell L, Plat F, Schork A, Smith B, Zanchetti A. Outcomes in hypertensive patients at high cardiovascular risk treated with regimens based on valsartan or amlodipine: the VALUE randomised trial. Lancet. 2004;363:2022-2031.
33. Ali MS, Schieffer B, Delafontaine P, Bernstein KE, Ling BN, Marrero MB. Angiotensin II stimulates tyrosine phosphorylation and activation of insulin receptor substrate 1 and protein-tyrosine phosphatase 1D in vascular smooth muscle cells. J Biol Chem. 1997;272:12373-12379.
34. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M, Shojima N, Ono H, Onishi Y, Fujishiro M, Katagiri H, Fukushima Y, Kikuchi M, Noguchi N, Aburatani H, Komuro I, Fujita T. Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension. 2002;40:872-879.
35. Gardner CD, Eguchi S, Reynolds CM, Eguchi K, Frank GD, Motley ED. Hydrogen peroxide inhibits insulin signaling in vascular smooth muscle cells. Exp Biol Med (Maywood). 2003;228:836-842.
36. Tirosh A, Potashnik R, Bashan N, Rudich A. Oxidative stress disrupts insulin-induced cellular redistribution of insulin receptor substrate-1 and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. A putative cellular mechanism for impaired protein kinase B activation and GLUT4 translocation. J Biol Chem. 1999;274:10595-10602.
37. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RA, Warnholtz A, Meinertz T, Griendling K, Harrison DG, Forstermann U, Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res. 2001;88:E14-E22.
38. Haber CA, Lam TK, Yu Z, Gupta N, Goh T, Bogdanovic E, Giacca A, Fantus IG. N-acetylcysteine and taurine prevent hyperglycemia-induced insulin resistance in vivo: possible role of oxidative stress. Am J Physiol Endocrinol Metab. 2003;285:E744-753.
39. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab. 2002;283:E413-E422.
40. Werner ED, Lee J, Hansen L, Yuan M, Shoelson SE. Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302. J Biol Chem. 2004;279:35298-35305.
41. Giraud J, Leshan R, Lee YH, White MF. Nutrient-dependent and insulin-stimulated phosphorylation of insulin receptor substrate-1 on serine 302 correlates with increased insulin signaling. J Biol Chem. 2004;279:3447-3454.
42. Lee AV, Gooch JL, Oesterreich S, Guler RL, Yee D. Insulin-like growth factor I-induced degradation of insulin receptor substrate 1 is mediated by the 26S proteasome and blocked by phosphatidylinositol 3′-kinase inhibition. Mol Cell Biol. 2000;20:1489-1496.
43. Rocic P, Seshiah P, Griendling KK. Reactive oxygen species sensitivity of angiotensin II-dependent translation initiation in vascular smooth muscle cells. J Biol Chem. 2003;278:36973-36979.