Angiotensin ii inhibits insulin-stimulated GLUT4 translocation and akt activation through tyrosine nitration-dependent mechanisms

PLoS ONE

Volumn 5, Issue 4, 2010, Pages 1-13

  Csibi, Alfredo ^a,d   Communi, David ^b   Müller, Nathalie ^a,e   Bottari, Serge P ^a,c  

^a UNIV GRENOBLE ALPES   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; FREE RADICAL; GLUCOSE TRANSPORTER 4; GLYCOGEN SYNTHASE KINASE 3ALPHA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYRICETIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN; PEROXYNITRITE; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE; THREONINE; TYROSINE; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, RAT; IRS2 PROTEIN, RAT; NITRATE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HORMONAL REGULATION; HORMONE ACTION; INSULIN RESISTANCE; MYOTUBE; NITRATION; NITRATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; SKELETAL MUSCLE; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; HUMAN; METABOLISM;

ANGIOTENSIN II; ANIMALS; CELLS, CULTURED; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NITRATES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RATS; TYROSINE;

EID: 77956308889     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010070     Document Type: Article

References (69)

1. Henriksen EJ (2007) Improvement of insulin sensitivity by antagonism of the renin-angiotensin system. Am J Physiol Regul Integr Comp Physiol 293: R974-980.
2. Coyle JD, Gardner SF, White CM (2004) The renal protective effects of angiotensin II receptor blockers in type 2 diabetes mellitus. Ann Pharmacother 38: 1731-1738.
3. Perkins JM, Davis SN (2008) The renin-angiotensin-aldosterone system: a pivotal role in insulin sensitivity and glycemic control. Curr Opin Endocrinol Diabetes Obes 15: 147-152.
4. Redon J, Cifkova R, Laurent S, Nilsson P, Narkiewicz K, et al. (2008) The metabolic syndrome in hypertension: European society of hypertension position statement. J Hypertens 26: 1891-1900.
5. Scheen AJ (2004) Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 2. Overview of physiological and biochemical mechanisms. Diabetes Metab 30: 498-505.
6. Sowers JR (2004) Insulin resistance and hypertension. Am J Physiol Heart Circ Physiol 286: H1597-1602.
7. Kintscher U, Bramlage P, Paar WD, Thoenes M, Unger T (2007) Irbesartan for the treatment of hypertension in patients with the metabolic syndrome: a sub analysis of the Treat to Target post authorization survey. Prospective observational, two armed study in 14,200 patients. Cardiovasc Diabetol 6: 12.
8. Blendea MC, Jacobs D, Stump CS, McFarlane SI, Ogrin C, et al. (2005) Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am J Physiol Endocrinol Metab 288: E353-359.
9. Shiuchi T, Iwai M, Li HS, Wu L, Min LJ, et al. (2004) Angiotensin II type-1 receptor blocker valsartan enhances insulin sensitivity in skeletal muscles of diabetic mice. Hypertension 43: 1003-1010.
10. Henriksen EJ, Jacob S, Kinnick TR, Teachey MK, Krekler M (2001) Selective angiotensin II receptor receptor antagonism reduces insulin resistance in obese Zucker rats. Hypertension 38: 884-890.
11. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, et al. (2006) Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 281: 35137-35146.
12. Richey JM, Ader M, Moore D, Bergman RN (1999) Angiotensin II induces insulin resistance independent of changes in interstitial insulin. Am J Physiol 277: E920-926.
13. Sloniger JA, Saengsirisuwan V, Diehl CJ, Kim JS, Henriksen EJ (2005) Selective angiotensin II receptor antagonism enhances whole-body insulin sensitivity and muscle glucose transport in hypertensive TG(mREN2)27 rats. Metabolism 54: 1659-1668.
14. Wenzel P, Schulz E, Oelze M, Muller J, Schuhmacher S, et al. (2008) AT1- receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med 45: 619-626.
15. Leiter LA, Lewanczuk RZ (2005) Of the renin-angiotensin system and reactive oxygen species Type 2 diabetes and angiotensin II inhibition. Am J Hypertens 18: 121-128.
16. Frank GD, Eguchi S, Yamakawa T, Tanaka S, Inagami T, et al. (2000) Involvement of reactive oxygen species in the activation of tyrosine kinase and extracellular signal-regulated kinase by angiotensin II. Endocrinology 141: 3120-3126.
17. Pinzar E, Wang T, Garrido MR, Xu W, Levy P, et al. (2005) Angiotensin II induces tyrosine nitration and activation of ERK1/2 in vascular smooth muscle cells. FEBS Lett 579: 5100-5104.
18. Pacher P, Szabo C (2006) Role of peroxynitrite in the pathogenesis of cardiovascular complications of diabetes. Curr Opin Pharmacol 6: 136-141.
19. Turko IV, Li L, Aulak KS, Stuehr DJ, Chang JY, et al. (2003) Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J Biol Chem 278: 33972-33977.
20. Szabo C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6: 662-680.
21. Ullrich V, Kissner R (2006) Redox signaling: bioinorganic chemistry at its best. J Inorg Biochem 100: 2079-2086.
22. Klotz LO, Schieke SM, Sies H, Holbrook NJ (2000) Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem J 352 Pt 1: 219-225.
23. Yasukawa T, Tokunaga E, Ota H, Sugita H, Martyn JA, et al. (2005) Snitrosylation- dependent inactivation of Akt/protein kinase B in insulin resistance. J Biol Chem 280: 7511-7518.
24. Carvalho-Filho MA, Ueno M, Hirabara SM, Seabra AB, Carvalheira JB, et al. (2005) S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes 54: 959-967.
25. Duplain H, Sartori C, Dessen P, Jayet PY, Schwab M, et al. (2008) Stimulation of peroxynitrite catalysis improves insulin sensitivity in high fat diet-fed mice. J Physiol 586: 4011-4016.
26. Sinha D, Bannergee S, Schwartz JH, Lieberthal W, Levine JS (2004) Inhibition of ligand-independent ERK1/2 activity in kidney proximal tubular cells deprived of soluble survival factors up-regulates Akt and prevents apoptosis. J Biol Chem 279: 10962-10972.
27. Kjeldsen SE, Julius S, Mancia G, McInnes GT, Hua T, et al. (2006) Effects of valsartan compared to amlodipine on preventing type 2 diabetes in high-risk hypertensive patients: the VALUE trial. J Hypertens 24: 1405-1412.
28. Navarro-Cid J, Maeso R, Perez-Vizcaino F, Cachofeiro V, Ruilope LM, et al. (1995) Effects of losartan on blood pressure, metabolic alterations, and vascular reactivity in the fructose-induced hypertensive rat. Hypertension 26: 1074-1078.
29. Redon J, Oliva MR, Tormos C, Giner V, Chaves J, et al. (2003) Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension 41: 1096-1101.
30. Whaley-Connell A, Sowers JR (2005) Hypertension management in type 2 diabetes mellitus: recommendations of the Joint National Committee VII. Endocrinol Metab Clin North Am 34: 63-75.
31. Sowers JR (2002) Hypertension, angiotensin II, and oxidative stress. NEngl J Med 346: 1999-2001.
32. Dorenkamp M, Riad A, Stiehl S, Spillmann F, Westermann D, et al. (2005) Protection against oxidative stress in diabetic rats: role of angiotensin AT(1) receptor and beta 1-adrenoceptor antagonism. Eur J Pharmacol 520: 179-187.
33. Fan Q, Liao J, Kobayashi M, Yamashita M, Gu L, et al. (2004) Candesartan reduced advanced glycation end-products accumulation and diminished itrooxidative stress in type 2 diabetic KK/Ta mice. Nephrol Dial Transplant 19: 3012-3020.
34. Adaikalakoteswari A, Balasubramanyam M, Rema M, Mohan V (2006) Differential gene expression of NADPH oxidase (p22phox) and hemoxygenase- 1 in patients with Type 2 diabetes and microangiopathy. Diabet Med 23: 666-674.
35. Avogaro A, Pagnin E, Calo L (2003) Monocyte NADPH oxidase subunit p22(phox) and inducible hemeoxygenase-1 gene expressions are increased in type II diabetic patients: relationship with oxidative stress. J Clin Endocrinol Metab 88: 1753-1759.
36. Kapur S, Bedard S, Marcotte B, Cote CH, Marette A (1997) Expression of nitric oxide synthase in skeletal muscle: a novel role for nitric oxide as a modulator of insulin action. Diabetes 46: 1691-1700.
37. Perreault M, Marette A (2001) Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 7: 1138-1143.
38. Ischiropoulos H, Gow A (2005) Pathophysiological functions of nitric oxidemediatedprotein modifications. Toxicology 208: 299-303.
39. Wattanapitayakul SK, Weinstein DM, Holycross BJ, Bauer JA (2000) Endothelial dysfunction and peroxynitrite formation are early events in angiotensin-induced cardiovascular disorders. Faseb J 14: 271-278.
40. Wayenberg JL, Ransy V, Vermeylen D, Damis E, Bottari SP (2009) Nitrated plasma albumin as a marker of nitrative stress and neonatal encephalopathy in perinatal asphyxia. Free Radic Biol Med 47: 975-982.
41. Ceriello A, Mercuri F, Quagliaro L, Assaloni R, Motz E, et al. (2001) Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 44: 834-838.
42. Ahmed N, Babaei-Jadidi R, Howell SK, Beisswenger PJ, Thornalley PJ (2005) Degradation products of proteins damaged by glycation, oxidation and nitration in clinical type 1 diabetes. Diabetologia 48: 1590-1603.
43. Turko IV, Murad F (2002) Protein nitration in cardiovascular diseases. Pharmacol Rev 54: 619-634.
44. Ceriello A, Quagliaro L, Catone B, Pascon R, Piazzola M, et al. (2002) Role of hyperglycemia in nitrotyrosine postprandial generation. Diabetes Care 25: 1439-1443.
45. Ceriello A, Assaloni R, Da Ros R, Maier A, Quagliaro L, et al. (2004) Effect of irbesartan on nitrotyrosine generation in non-hypertensive diabetic patients. Diabetologia 47: 1535-1540.
46. Pueyo ME, Arnal JF, Rami J, Michel JB (1998) Angiotensin II stimulates the production of NO and peroxynitrite in endothelial cells. Am J Physiol 274: C214-220.
47. Guo W, Adachi T, Matsui R, Xu S, Jiang B, et al. (2003) Quantitative assessment of tyrosine nitration of manganese superoxide dismutase in angiotensin II-infused rat kidney. Am J Physiol Heart Circ Physiol 285: H1396-1403.
48. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, et al. (2008) Angiotensin IIinduced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab 294: E345-351.
49. Daiber A, Schildknecht S, Muller J, Kamuf J, Bachschmid MM, et al. (2009) Chemical model systems for cellular nitros(yl)ation reactions. Free Radic Biol Med 47: 458-467.
50. Frein D, Schildknecht S, Bachschmid M, Ullrich V (2005) Redox regulation: a new challenge for pharmacology. Biochem Pharmacol 70: 811-823.
51. Beckman JS, Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271: C1424-1437.
52. Kamisaki Y, Wada K, Bian K, Balabanli B, Davis K, et al. (1998) An activity in rat tissues that modifies nitrotyrosine-containing proteins. Proc Natl Acad Sci U S A 95: 11584-11589.
53. Koeck T, Fu X, Hazen SL, Crabb JW, Stuehr DJ, et al. (2004) Rapid and selective oxygen-regulated protein tyrosine denitration and nitration in mitochondria. J Biol Chem 279: 27257-27262.
54. Calleja V, Laguerre M, Larijani B (2009) 3-D structure and dynamics of protein kinase B-new mechanism for the allosteric regulation of an AGC kinase. J Chem Biol 2: 11-25.
55. Conus NM, Hannan KM, Cristiano BE, Hemmings BA, Pearson RB (2002) Direct identification of tyrosine 474 as a regulatory phosphorylation site for the Akt protein kinase. J Biol Chem 277: 38021-38028.
56. Nolen B, Taylor S, Ghosh G (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15: 661-675.
57. Izawa Y, Yoshizumi M, Fujita Y, Ali N, Kanematsu Y, et al. (2005) ERK1/2 activation by angiotensin II inhibits insulin-induced glucose uptake in vascular smooth muscle cells. Exp Cell Res 308: 291-299.
58. Corbould A, Zhao H, Mirzoeva S, Aird F, Dunaif A (2006) Enhanced mitogenic signaling in skeletal muscle of women with polycystic ovary syndrome. Diabetes 55: 751-759.
59. Zhang Y, Brovkovych V, Brovkovych S, Tan F, Lee BS, et al. (2007) Dynamic receptor-dependent activation of inducible nitric-oxide synthase by ERKmediated phosphorylation of Ser745. J Biol Chem 282: 32453-32461.
60. Brovkovych V, Zhang Y, Brovkovych S, Minshall RD, Skidgel RA (2009) A novel pathway for receptor-mediated post-translational activation of inducible nitric oxide synthase. J Cell Mol Med.
61. Franke TF (2008) Intracellular signaling by Akt: bound to be specific. Sci Signal 1: pe29.
62. Kone BC, Kuncewicz T, Zhang W, Yu ZY (2003) Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. Am J Physiol Renal Physiol 285: F178-190.
63. El Bekay R, Alba G, Reyes ME, Chacon P, Vega A, et al. (2007) Rac2 GTPase activation by angiotensin II is modulated by Ca2+/calcineurin and itogenactivated protein kinases in human neutrophils. J Mol Endocrinol 39: 351-363.
64. Gupta SK, Vlahakis NE (2009) Integrin alpha9beta1 mediates enhanced cell migration through nitric oxide synthase activity regulated by Src tyrosine kinase. J Cell Sci 122: 2043-2054.
65. Manivet P, Mouillet-Richard S, Callebert J, Nebigil CG, Maroteaux L, et al. (2000) PDZ-dependent activation of nitric-oxide synthases by the serotonin 2B receptor. J Biol Chem 275: 9324-9331.
66. Kintscher U, Foryst-Ludwig A, Unger T (2008) Inhibiting angiotensin type 1 receptors as a target for diabetes. Expert Opin Ther Targets 12: 1257-1263.
67. Yusuf S, Teo KK, Pogue J, Dyal L, Copland I, et al. (2008) Telmisartan, ramipril, or both in patients at high risk for vascular events. N Engl J Med 358: 1547-1559.
68. Barnett AH (2005) Preventing renal complications in diabetic patients: the Diabetics Exposed to Telmisartan And enalaprIL (DETAIL) study. Acta Diabetol 42 Suppl 1: S42-49.
69. Yonemitsu S, Nishimura H, Shintani M, Inoue R, Yamamoto Y, et al. (2001) Troglitazone induces GLUT4 translocation in L6 myotubes. Diabetes 50: 1093-1101.