Nitric oxide attenuates insulin- or IGF-I-stimulated aortic smooth muscle cell motility by decreasing H2O2 levels: Essential role of cGMP

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 6 55-6, 2004, Pages

  Zhuang, Daming ^a   Ceacareanu, Alice Corina ^a   Lin, Yi ^a   Ceacareanu, Bogdan ^a   Dixit, Madhulika ^a   Chapman, Kenneth E ^a   Waters, Christopher M ^a   Rao, Gadiparthi N ^a   Hassid, Aviv ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Akt; Antioxidant; NAD(P)H oxidase; Vascular remodeling

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 (4 CHLOROPHENYLTHIO) CYCLIC GMP; ACETYLCYSTEINE; ANTIOXIDANT; CATALASE; CYCLIC GMP; CYCLIC GMP DERIVATIVE; DIPHENYLIODONIUM SALT; HYDROGEN PEROXIDE; INSULIN; NITRIC OXIDE; NITRIC OXIDE DONOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; AORTA MEDIA; ARTICLE; ATTENUATION; CELL MOTILITY; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; ENZYME MECHANISM; FEMALE; INHIBITION KINETICS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; VASCULAR DISEASE; VASCULAR REMODELING;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; AORTA, THORACIC; CATALASE; CELL MOVEMENT; CELLS, CULTURED; CYCLIC GMP; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; GUANYLATE CYCLASE; HYDROGEN PEROXIDE; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MUSCLE, SMOOTH, VASCULAR; NADPH OXIDASE; NITRIC OXIDE; OXADIAZOLES; OXIDANTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 2542439727     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.01118.2003     Document Type: Article

References (50)

1. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, and Rhee SG. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 272: 217-221, 1997.
2. Begum N, Ragolia L, Rienzie J, McCarthy M, and Duddy N. Regulation of mitogen-activated protein kinase phosphatase-1 induction by insulin in vascular smooth muscle cells. Evaluation of the role of the nitric oxide signaling pathway and potential defects in hypertension. J Biol Chem 273: 25164-25170, 1998.
3. Brown MR, Miller FJ Jr, Li WG, Ellingson AN, Mozena JD, Chatterjee P, Engelhardt JF, Zwacka RM, Oberley LW, Fang X, Spector AA, and Weintraub NL. Overexpression of human catalase inhibits proliferation and promotes apoptosis in vascular smooth muscle cells. Circ Res 85: 524-533, 1999.
4. Buckley DA, Cheng A, Kiely PA, Tremblay ML, and O'Connor R. Regulation of insulin-like growth factor type I (IGF-I) receptor kinase activity by protein tyrosine phosphatase 1B (PTP-1B) and enhanced IGF-I-mediated suppression of apoptosis and motility in PTP-1B-deficient fibroblasts. Mol Cell Biol 22: 1998-2010, 2002.
5. Chang Y, Ceacareanu B, Dixit M, Sreejayan N, and Hassid A. Nitric oxide-induced motility in aortic smooth muscle cells: role of protein tyrosine phosphatase SHP-2 and GTP-binding protein Rho. Circ Res 91: 390-397, 2002.
6. Christiansen NO, Larsen CS, and Esmann V. A study on the role of protein kinase C and intracellular calcium in the activation of superoxide generation. Biochim Biophys Acta 971: 317-324, 1988.
7. Clancy RM, Leszczynska-Piziak J, and Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 90: 1116-1121, 1992.
8. 2+ by atriopeptin and 8-bromo-cyclic GMP is mediated by cyclic GMP-dependent protein kinase. J Biol Chem 264: 1146-1155, 1989.
9. Dahlgren C, Johansson A, Lundqvist H, Bjerrum OW, and Borregaard N. Activation of the oxygen-radical-generating system in granules of intact human neutrophils by a calcium ionophore (ionomycin). Biochim Biophys Acta 1137: 182-188, 1992.
10. Delafontaine P and Ku L. Reactive oxygen species stimulate insulin-like growth factor I synthesis in vascular smooth muscle cells. Cardiovasc Res 33: 216-222, 1997.
11. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, and Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 253: 1129-1132, 1991.
12. Fujii H, Ichimori K, Hoshiai K, and Nakazawa H. Nitric oxide inactivates NADPH oxidase in pig neutrophils by inhibiting its assembling process. J Biol Chem 272: 32773-32778, 1997.
13. Garg UC and Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 83: 1774-1777, 1989.
14. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, and Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48: 184-188, 1995.
15. Griendling KK, Minieri CA, Ollerenshaw JD, and Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74: 1141-1148, 1994.
16. Guzik TJ, West NE, Pillai R, Taggart DP, and Channon KM. Nitric oxide modulates superoxide release and peroxynitrite formation in human blood vessels. Hypertension 39: 1088-1094, 2002.
17. Hassid A. Atriopeptin II decreases cytosolic free Ca in cultured vascular smooth muscle cells. Am J Physiol Cell Physiol 251: C681-C686, 1986.
18. Hassid A, Yao J, and Huang S. NO alters cell shape and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B activation. Am J Physiol Heart Circ Physiol 277: H1014-H1026, 1999.
19. Hsueh WA and Law RE. Cardiovascular risk continuum: implications of insulin resistance and diabetes. Am J Med 105: 4S-14S, 1998.
20. Indolfi C, Torella D, Cavuto L, Davalli AM, Coppola C, Esposito G, Carriero MV, Rapacciuolo A, Di Lorenzo E, Stabile E, Perrino C, Chieffo A, Pardo F, and Chiariello M. Effects of balloon injury on neointimal hyperplasia in streptozotocin-induced diabetes and in hyperinsulinemic nondiabetic pancreatic islet-transplanted rats. Circulation 103: 2980-2986, 2001.
21. Khorsandi MJ, Fagin JA, Giannella-Neto D, Forrester JS, and Cercek B. Regulation of insulin-like growth factor-I and its receptor in rat aorta after balloon denudation. Evidence for local bioactivity. J Clin Invest 90: 1926-1931, 1992.
22. Kooy NW, Royall JA, and Ischiropoulos H. Oxidation of 2′,7′-dichlorofluorescin by peroxynitrite. Free Radic Res 27: 245-254, 1997.
23. Kubo T, Saito E, Hanada M, Kambe T, and Hagiwara Y. Evidence that angiotensin II, endothelins and nitric oxide regulate mitogen-activated protein kinase activity in rat aorta. Eur J Pharmacol 347: 337-346, 1998.
24. Lee SR, Kwon KS, Kim SR, and Rhee SG. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 273: 15366-15372, 1998.
25. Loesberg C, van Wijk R, Zandbergen J, van Aken WG, van Mourik JA, and de Groot PG. Cell cycle-dependent inhibition of human vascular smooth muscle cell proliferation by prostaglandin E1. Exp Cell Res 160: 117-125, 1985.
26. Mahadev K, Wu X, Zilbering A, Zhu L, Lawrence JT, and Goldstein BJ. Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes. J Biol Chem 276: 48662-48669, 2001.
27. Majesky MW, Giachelli CM, Reidy MA, and Schwartz SM. Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res 71: 759-768, 1992.
28. Munzel T, Afanas'ev IB, Kleschyov AL, and Harrison DG. Detection of superoxide in vascular tissue. Arterioscler Thromb Vasc Biol 22: 1761-1768, 2002.
29. Pagano PJ, Ito Y, Tornheim K, Gallop PM, Tauber AI, and Cohen RA. An NADPH oxidase superoxide-generating system in the rabbit aorta. Am J Physiol Heart Circ Physiol 268: H2274-H2280, 1995.
30. Parinandi NL, Kleinberg MA, Usatyuk PV, Cummings RJ, Pennathur A, Cardounel AJ, Zweier JL, Garcia JG, and Natarajan V. Hyperoxia-induced NAD(P)H oxidase activation and regulation by MAP kinases in human lung endothelial cells. Am J Physiol Lung Cell Mol Physiol 284: L26-L38, 2003.
31. Phelps DT, Deneke SM, Daley DL, and Fanburg BL. Elevation of glutathione levels in bovine pulmonary artery endothelial cells by N-acetylcysteine. Am J Respir Cell Mol Biol 7: 293-299, 1992.
32. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, and Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/ NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 97: 1916-1923, 1996.
33. Rao GN. Hydrogen peroxide induces complex formation of SHC-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signal-regulated protein kinases group of mitogen-activated protein kinases. Oncogene 13: 713-719, 1996.
34. Rhee SG, Bae YS, Lee SR, and Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000: E1, 2000.
35. Rodenas J, Mitjavila MT, and Carbonell T. Nitric oxide inhibits superoxide production by inflammatory polymorphonuclear leukocytes. Am J Physiol Cell Physiol 274: C827-C830, 1998.
36. Rubanyi GM, Ho EH, Cantor EH, Lumma WC, and Botelho LH. Cytoprotective function of nitric oxide: inactivation of superoxide radicals produced by human leukocytes. Biochem Biophys Res Commun 181: 1392-1397, 1991.
37. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, and Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest 101: 731-736, 1998.
38. Schneider JE, Berk BC, Gravanis MB, Santoian EC, Cipolla GD, Tarazona N, Lassegue B, and King SB 3rd. Probucol decreases neointimal formation in a swine model of coronary artery balloon injury. A possible role for antioxidants in restenosis. Circulation 88: 628-637, 1993.
39. Sharma RV, Tan E, Fang S, Gurjar MV, and Bhalla RC. NOS gene transfer inhibits expression of cell cycle regulatory molecules in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 276: H1450-H1459, 1999.
40. Shi Y, Niculescu R, Wang D, Patel S, Davenpeck KL, and Zalewski A. Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler Thromb Vasc Biol 21: 739-745, 2001.
41. Skatchkov MP, Sperling D, Hink U, Mulsch A, Harrison DG, Sindermann I, Meinertz T, and Munzel T. Validation of lucigenin as a chemiluminescent probe to monitor vascular superoxide as well as basal vascular nitric oxide production. Biochem Biophys Res Commun 254: 319-324, 1999.
42. Sreejayan N, Lin Y, and Hassid A. NO attenuates insulin signaling and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B-mediated mechanism. Arterioscler Thromb Vasc Biol 22: 1086-1092, 2002.
43. 2 for platelet-derived growth factor signal transduction. Science 270: 296-299, 1995.
44. Suzuki LA, Poot M, Gerrity RG, and Bornfeldt KE. Diabetes accelerates smooth muscle accumulation in lesions of atherosclerosis: lack of direct growth-promoting effects of high glucose levels. Diabetes 50: 851-860, 2001.
45. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, and Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol 22: 21-27, 2002.
46. Van Belle E, Bauters C, Hubert E, Bodart JC, Abolmaali K, Meurice T, McFadden EP, Lablanche JM, and Bertrand ME. Restenosis rates in diabetic patients: a comparison of coronary stenting and balloon angioplasty in native coronary vessels. Circulation 96: 1454-1460, 1997.
47. Von der Leyen HE, Gibbons GH, Morishita R, Lewis NP, Zhang L, Nakajima M, Kaneda Y, Cooke JP, and Dzau VP. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci USA 92: 1137-1141, 1995.
48. Walchli S, Curchod ML, Gobert RP, Arkinstall S, and Hooft van Huijsduijnen R. Identification of tyrosine phosphatases that dephosphorylate the insulin receptor. A brute force approach based on " substrate-trapping" mutants. J Biol Chem 275: 9792-9796, 2000.
49. Yumi K, Fagin JA, Yamashita M, Fishbein MC, Shah PK, Kaul S, Niu W, Nilsson J, and Cercek B. Direct effects of somatostatin analog octreotide on insulin-like growth factor-I in the arterial wall. Lab Invest 76: 329-338, 1997.
50. Zhu B, Zhao G, Witte DP, Hui DY, and Fagin JA. Targeted overexpression of IGF-I in smooth muscle cells of transgenic mice enhances neointimal formation through increased proliferation and cell migration after intraarterial injury. Endocrinology 142: 3598-3606, 2001.