Xanthine oxidase-derived extracellular superoxide anions stimulate activator protein 1 activity and hypertrophy in human vascular smooth muscle via c-Jun N-terminal kinase and p38 mitogen-activated protein kinases

Journal of Hypertension

Volumn 25, Issue 3, 2007, Pages 609-618

  Matesanz, Nuria ^a   Lafuente, Nuria ^a   Azcutia, Verónica ^a   Martín, Daniel ^b   Cuadrado, Antonio ^b   Nevado, Julián ^c   Rodríguez Mañas, Leocadio ^c   Sánchez Ferrer, Carlos F ^a   Peiró, Concepción ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c HOSPITAL UNIVERSITARIO DE GETAFE   (Spain)

Author keywords

Activator protein 1; Allopurinol; Hypertrophy; Mitogen activated protein kinases; Superoxide anions; Vascular smooth muscle; Xanthine oxidase

Indexed keywords

ALLOPURINOL; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR AP 1; XANTHINE; XANTHINE OXIDASE;

AORTA MEDIA; ARTICLE; CARDIOVASCULAR DISEASE; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CELL SIZE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MODIFICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MUSCLE GROWTH; MUSCLE HYPERTROPHY; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SMOOTH MUSCLE FIBER; TRANSIENT TRANSFECTION; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

EID: 33846804182     PISSN: 02636352     EISSN: None     Source Type: Journal    
DOI: 10.1097/HJH.0b013e328013e7c4     Document Type: Article

References (49)

1. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000; 87:840-844.
2. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature. Molecular and cellular mechanisms. Hypertension 2003; 42:1075-1081.
3. Mueller CFH, Laude K, McNally JS, Harrison DG. Redox mechanisms in blood vessels. Arterioscler Thromb Vasc Biol 2005; 25:274-278.
4. Berry CB, Hamilton CA, Brosnan MJ, Magil FG, Berg GA, McMurray JJV, et al. Investigation into the sources of superoxide in human blood vessels. Angiotensin II increases superoxide production in human internal mammary arteries. Circulation 2000; 101:2206-2212.
5. Spiekermann S, Landmesser U, Dikalov S, Bredt M, Gamez G, Tatge H, et al. Electro spin resonance characterization of vascular xanthine and NAD(P)H oxidase activity in patients with coronary artery disease. Relation to endothelium-dependent vasodilation. Circulation 2003; 107:1383-1389.
6. Berry CE, Hare JM. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms ans pathohysiological implications. J Physiol 2004; 555:589-606.
7. Dikalova A, Clempus R, Lassegue B, Cheng G, McCoy J, Dikalov S, et al. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 2005; 112:2668-2676.
8. Peiró C, Matesanz N, Nevado J, Lafuente N, Cercas E, Azcutia V, et al. Glycosylated human oxyhaemoglobin activates nuclear factor-kappaB and activator protein-1 in cultured human aortic smooth muscle. Br J Pharmacol 2003; 140:681-690.
9. Crapo JD, McCord JM, Fridovich I. Preparation and assay of superoxide dismutases. Methods Enzymol 1978; 53:382-393.
10. Bunik VI, Sievers C. Inactivation of the 2-oxo acid dehydrogenase complexes upon generation of intrinsic radical species. Eur J Biochem 2002; 269:5004-5015.
11. Peiró C, Vallejo S, Nevado J, Angulo J, Llergo JL, Cercas E, et al. Pharmacological interference of vascular smooth muscle cell hypertrophy induced by glycosylated human oxyhaemoglobin. Eur J Pharmacol 1999; 386:317-321.
12. Peiró C, Llergo JL, Angulo J, Lopez-Novoa JM, Rodríguez- Lopez A, Rodríguez-Mañas L, et al. Effects of captopril, losartan, and nifedipine on cell hypertrophy of cultured vascular smooth muscle from hypertensive Ren-2 transgenic rats. Br J Pharmacol 1997; 121:1438-1444.
13. Berk BC, Vekshtein V, Gordon HM, Tsuda T. Angiotensin II-stimulated protein synthesis in cultured vascular smooth muscle cells. Hypertension 1989; 13:305-314.
14. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, et al. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3 kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical, carnosol. J Biol Chem 2003; 279:8919-8929.
15. Cai H, Griendling KK, Harrison DG. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 2003; 24:471-478.
16. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001; 22:153-183.
17. 2 in vascular smooth muscle cells: potential involvement in vascular disease. Int J Mol Med 2003; 11:229-234.
18. Swei A, Lacy F, Delano FA, Parks DA, Schmid-Schonbein GW. A mechanism of oxygen free radical production in the Dahl hypertensive rat. Microcirculation 1999; 6:179-187.
19. Ulker S, McMaster D, McKeown PP, Bayraktutan U. Impaired activities of antioxidant enzymes elicit endothelial dysfunction in spontaneous hypertensive rats despite enhanced vascular nitric oxide generation. Cardiovasc Res 2003; 59:488-500.
20. Cardillo C, Kilcoyne CM, Cannon RO III, Quyyumi AA, Panza JA. Xanthine oxidase inhibition with oxypurinol improves endothelial vasodilator function in hypercholesterolemic but not in hypertensive patients. Hypertension 1997; 30:57-63.
21. Butler R, Morris AD, Belch JJ, Hill A, Struthers AD. Allopurinol normalizes endothelial dysfunction in type 2 diabetics with mild hypertension. Hypertension 2000; 35:746-751.
22. Guthikonda S, Sinkey C, Barenz T, Haynes WG. Xanthine oxidase inhibition reverses endothelial dysfunction in heavy smokers. Circulation 2003; 107:416-421.
23. Guzik TJ, West NEJ, Black E, McDonald D, Ratnatunga C, Pillai R, et al. Vascular superoxide production by NAD(P)H oxidase. Association with endothelial dysfunction and clinical risk factors. Circ Res 2000; 86:e85-e90.
24. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, et al. 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.
25. Peiró C, Angulo J, Rodríguez-Mañas L, Llergo JL, Vallejo S, Cercas E, et al. Vascular smooth muscle cell hypertrophy induced by glycosylated human oxyhaemoglobin. Br J Pharmacol 1998; 125:637-644.
26. Li PF, Dietz R, Harsdorf R. Differential effect of hydrogen peroxide and superoxide anion on apoptosis and proliferation of vascular smooth muscle cells. Circulation 1997; 96:3602-3609.
27. Nickenig G, Baudler S, Muller C, Werner C, Werner N, Welzel H, et al. Redox-sensitive vascular smooth muscle cell proliferation is mediated by GKLF and Id3 in vitro and in vivo. FASEB J 2002; 16:1077-1086.
28. Yoshizumi M, Tsuchiya K, Suzaki Y, Kirima K, Kyaw M, Moon JH, et al. Quercetin glucuronide prevents VSMC hypertrophy by angiotensin II via the inhibition of JNK and AP-1 signaling pathway. Biochem Biophys Res Commun 2002; 293:1458-1465.
29. Viedt C, Fei J, Krieger-Brauer HI, Brandes RP, Teupser D, Kamimura M, et al. Role of p22phox in angiotensin II and platelet-derived growth factor AA induced activator protein 1 activation in vascular smooth muscle cells. J Mol Med 2004; 82:31-38.
30. Morita N, Iizuka K, Murakami T, Kawaguchi H. N-terminal kinase, and c-Src are activated in human aortic smooth muscle cells by pressure stress. Mol Cell Biochem 2004; 262:71-78.
31. Naveilhan P, Neveu I, Jehan F, Baudet C, Wion D, Brachet P. Reactive oxygen species influence nerve growth factor synthesis in primary rat astrocytes. J Neurochem 1994; 62:2178-2186.
32. Singh N, Aggarwal S. The effect of active oxygen generated by xanthine/xanthine oxidase on genes and signal transduction in mouse epidermal JB6 cells. Int J Cancer 1995; 62:107-114.
33. Yoshizumi M, Tsuchiya K, Kirima K, Kyaw M, Suzaki Y, Tamaki T. Quercetin inhibits Shc- and phosphatidylinositol 3-kinase-mediated c-Jun N-terminal kinase activation by angiotensin II in cultured rat aortic smooth muscle cells. Mol Pharmacol 2001; 60:656-665.
34. Taniyama Y, Ushio-Fukai M, Hitomi H, Rocic P, Kingsley MJ, Pfahnl C, et al. Role of p38 MAPK and MAPKAPK-2 in angiotensin II-induced Akt activation in vascular smooth muscle cells. Am J Physiol Cell Physiol 2004; 287:C494-C499.
35. Haider UG, Sorescu D, Griendling KK, Vollmar AM, Dirsch VM. Resveratrol suppresses angiotensin II-induced Akt/protein kinase B and p70 S6 kinase phosphorylation and subsequent hypertrophy in rat aortic smooth muscle cells. Mol Pharmacol 2002; 62:772-777.
36. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001; 81:807-869.
37. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nature Cell Biol 2002; 4:E131-E136.
38. Whitmarsh AJ, Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 1996; 74:589-607.
39. Suzuki E, Satonaka H, Nishimatsu H, Oba S, Takeda R, Omata M, et al. Myocyte enhancer factor 2 mediates vascular inflammation via the p38-dependent pathway. Circ Res 2004; 95:42-49.
40. Suzuki E, Nishimatsu H, Satonaka H, Walsh K, Goto A, Omata M, et al. Angiotensin II induces myocyte enhancer factor 2- and calcineurin/nuclear factor of activated T cell-dependent transcriptional activation in vascular myocytes. Circ Res 2002; 90:1004-1011.
41. Kalyankrishna S, Malik KU. Norepinephrine-induced stimulation of p38 mitogen-activated protein kinase is mediated by arachidonic acid metabolites generated by activation of cytosolic phospholipase A(2) in vascular smooth muscle cells. J Pharmacol Exp Ther 2003; 304:761-772.
42. Fukuyama K, Ichiki T, Ono H, Tokunou T, Iino N, Masuda S, et al. cAMP-response element-binding protein mediates prostaglandin F2alpha-induced hypertrophy of vascular smooth muscle cells. Biochem Biophys Res Commun 2005; 338:910-918.
43. Shin HJ, Oh J, Kang SM, Lee JH, Shin MJ, Hwang KC, et al. Leptin induces hypertrophy via p38 mitogen-activated protein kinase in rat vascular smooth muscle cells. Biochem Biophys Res Commun 2005; 329:18-24.
44. Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, Griendling KK. p22Phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 1996; 27:23317-23321.
45. Kuppusamy P, Zweier JL. Characterization of free radical by xanthine. Evidence for hydroxyl radical generation. J Biol Chem 1989; 264:9880-9884.
46. Courtois M, Maupoil V, Fantini E, Durot I, Javouhey-Donzel A, Athias P, et al. Correlation between direct ESR spectroscopic measurements and electromechanical and biochemical assessments of exogenous free radical injury in isolated rat cardiac myocytes. Free Radic Biol Med 1998; 24:121-131.
47. Nakai K, Kadiiska MB, Jiang JJ, Stadler K, Mason RP. Free radical production requires both inducible nitric oxide synthase and xanthine oxidase in LPS-treated skin. Proc Natl Acad Sci U S A 2006; 103:4616-4621.
48. Minhas KM, Saraiva RM, Schuleri KH, Lehrke S, Zheng M, Saliaris AP, et al. Xanthine oxidoreductase inhibition causes reverse remodeling in rats with dilated cardiomyopathy. Circ Res 2006; 98:271-279.
49. Engberding N, Spiekermann S, Schaefer A, Heineke A, Wiencke A, Muller M, et al. Allopurinol attenuates left ventricular remodeling and dysfunction after experimental myocardial infarction: a new action for an old drug? Circulation 2004; 110:2175-2179.