Role of NADPH oxidase in atherosclerosis

Future Cardiology

Volumn 5, Issue 1, 2009, Pages 83-92

  Violi, Francesco ^a   Basili, Stefania ^a   Nigro, Carmen ^a   Pignatelli, Pasquale ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Atherosclerosis; Endothelial dysfunction; NADPH oxidase; NOX; ROS

Indexed keywords

APOCYNIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PR 39; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2 INHIBITOR; SUPEROXIDE; UNCLASSIFIED DRUG; VAS 2870;

ARTERY INTIMA PROLIFERATION; ATHEROSCLEROSIS; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME POLYMORPHISM; ENZYME STRUCTURE; HUMAN; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; RISK ASSESSMENT; RISK FACTOR; UPREGULATION;

ATHEROSCLEROSIS; BIOLOGICAL MARKERS; BLOOD VESSELS; DISEASE PROGRESSION; HUMANS; NADPH OXIDASE; REACTIVE OXYGEN SPECIES;

EID: 66949169956     PISSN: 14796678     EISSN: 17448298     Source Type: Journal    
DOI: 10.2217/14796678.5.1.83     Document Type: Review

References (107)

1. Sorescu D, Weiss D, Lassegue B et al.: Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105, 1429-1435 (2002).
2. Galis ZS, Muszynski M, Sukhova GK et al.: Enhanced expression of vascular matrix metalloproteinases induced in vitro by cytokines and in regions of human atherosclerotic lesions. Ann. NY Acad. Sci. 748, 501-507 (1995).
3. Rajagopalan S, Meng XP, Ramasamy S et al.: Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. J. Clin. Invest. 98, 2572-2579 (1996).
4. Marui N, Offermann MK, Swerlick R et al.: Vascular cell-adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant sensitive mechanism in human vascular endothelial cells. J. Clin. Invest. 92, 1866-1874 (1993).
5. Arai T, Kelly SA, Brengman ML et al.: Ambient but not incremental oxidant generation effects intercellular adhesion molecule 1 induction by turnout necrosis factor a in endothelium. Biochem. J. 331, 853-861 (1998).
6. Ray R, Shah AM: NADPH oxidase and endothelial cell function. Clinical Science 109, 217-226 (2005).
7. Griendling KK, Sorescu D, Ushio-Fukai M: NADPH oxidase: role in cardiovascular biology and disease. Circ. Res. 86, 494-501 (2000).
8. Lambeth JD: Nox enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189 (2004).
9. Babior BM, Lambeth JD, Nauseef W: The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344 (2002).
10. DeLeo FR, Quinn MT: Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J. Leukocyte Biol. 60, 677-691 (1996).
11. Lassegue B, Clempus RE: Vascular NAD (P)H oxidases: specific features, expression, and regulation. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 285, R277-R297 (2003).
12. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW: Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74, 1141-1148 (1994).
13. Bayrakturan U, Blayney L, Shah AM: Molecular characterization and localization of the NAD(P)H oxidase components gp91-phox and p22-phox in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 20, 1903-1911 (2000).
14. Gorlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R: A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ. Res. 87, 26-32 (2000).
15. Pagano PJ: Vascular gp91phox: beyond the endothelium. Circ. Res. 87, 1-3 (2000).
16. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM: Pivotal role of a gp91phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 105, 293-296 (2002).
17. Pignatelli P, Sanguigni V, Lenti L et al.: gp91phox-dependent expression of platelet CD40 ligand. Circulation 110, 1326-1329 (2004).
18. Suh YA, Arnold RS, Lassegue B et al.: Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82 (1999).
19. Cheng G, Cao Z, Xu X, van Meir EG, Lambeth JD: Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140 (2001).
20. Bedard K, Krause KH: The NOX family of ROS-generating NADPH oxidases: phisiology and pathophysiology. Physiol. Rev. 87, 245-313 (2007).
21. Takeya R, Ueno N, Kami K et al.: Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases. J. Biol. Chem. 278, 25234-25246 (2003).
22. Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R, Brandes RP: Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279, 45935-45941 (2004).
23. 2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J. Biol. Chem. 276, 37594-37601 (2001).
24. Cheng G, Ritsick D, Lambeth JD: Nox3 regulation by NOXO1, p47phox, and p67phox. J. Biol. Chem. 279, 34250-34255 (2004).
25. Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH: NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279, 46065-46072 (2004).
26. Guzik TJ, Harrison DG: Vascular NADPH oxidases as drug targets for novel antioxidant strategies. Drug Discovery Today 11, 524-533 (2006).
27. Li JM, Shah AM: Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277, 19952-19960 (2002).
28. Dikalov SI, Dikalova AE, Bikineyeva AT et al.: Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated supeoxide and hydrogen peroxide production. Free Radic. Biol. Med. 45, 1340-1351 (2008).
29. Jones SA, O'Donnell VB, Wood JD, Broughton JP, Hughes EJ, Jones OT: Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 271, H1626-H1634 (1996).
30. Li JM, Shah AM: Differential NADPH versus NADH-dependent superoxide production by phagocyte-type endothelial cell NADPH oxidase. Cardiovasc. Res. 52, 477-486 (2001).
31. Cave AC, Brewer AC, Narayanapanicker A et al.: NADPH oxidases in cardovascular health and disease. Antioxid. Redox Signal. 8, 691-728 (2006).
32. Griendling KK, FitzGerald GA: Oxidative stress and cardiovascular injury part I: basic mechanisms and in vivo monitoring of ROS. Circulation 108, 1912-1916 (2003).
33. Lu D, Maulik N, Moraru II et al.: Molecular adaptation of vascular endothelial cells to oxidative stress. Am. J. Physiol. 264, C715-C722 (1993).
34. Kunsch C, Medford RM: Oxidative stress as a regulator of gene expression in the vasculature. Circ. Res. 85, 753-766 (1999).
35. Dworakowski R, Alom-Ruiz SP, Shan AM: NADPH oxidase-derived reactive oxygen species in the regulation of endothelial phenotype. Pharmacological Reports 60, 21-28 (2008).
36. Napoli C, de Nigris E, Palinski W: Multiple role of reactive oxygen species in the arterial wall. J. Cell. Biochem. 82, 674-682 (2001).
37. Matsuno K, Yamada H, Iwata K et al.: Nox1 is involved in angiotensin II-mediated hypertension a study in nox1 -deficient mice. Circulation 112, 2677-2685 (2005).
38. Jung O, Schreiber JG, Geiger H, Pedrazzini T, Busse R, Brandes RP: gp91phox-containing NADPH oxidase mediates endothelial dysfunction in renovascular hypertension. Circulation 109, 1795-1801 (2004).
39. Violi F, Sanguigni V, Loffredo L et al.: Nox2 is determinant for ischemia-induced oxidative stress and arterial vasodilatation: a pilot study in patients with hereditary Nox2 deficiency. Arterioscler. Thromb. Vasc. Biol. 26, E131-E132 (2006).
40. Cai H, Harrison DG: Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87, 840-844 (2000).
41. Van Buul JD, Fernandez-Boria M, Anthony EC, Hordijk PL: Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxid. Redox Signal. 7, 308-317 (2005)
42. Lassegue B, Sorescu D, Szocs K et al.: Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88, 888-894 (2001).
43. Fukui T, Ishizaka N, Rajagopalan S: p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ. Res. 80, 45-51 (1997).
44. Griendling KK, Ushio-Fukai M: Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept. 91, 21-27 (2000)
45. Wang HD, Xu S, Johns DG et al.: Role of NADPH oxidase in the vascular hypertrophic and oxidative stress response to angiotensin II in mice. Circ. Res. 88, 947-953 (2001).
46. Dikalova A, Clempus R, Lassegue B et al.: Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112, 2668-2676 (2005).
47. Laude K, Cai H, Fink B et al.: Hemodynamic and biochemical adaptations to vascular smooth muscle overexpression of p22phox in mice. Am. J. Physiol. Heart Circ. Physiol. 288, H7-H12 (2005).
48. Rajagopalan S, Kurz S, Münzel T et al.: Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. J. Clin. Invest. 97, 1916-1923 (1996).
49. 2 production, vascular tone, and mitogen-activated protein kinase activation. Circulation 109, 1307-1313 (2004).
50. Landmesser U, Cai H, Dikalov S et al.: Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40, 511-515 (2002).
51. Doughan AK, Harrison DG, Dikalov SI: Molecular mechanisms of angiotensin II- medieted mithochondial dysfunction. Linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Rec. 102, 488-496 (2008).
52. Gauthier TW, Scalia R, Murohara T, Guo J-P, Lefer AM: Nitric oxide protects against leukocyte-endothelium interactions in the early stages of hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 15, 1652-1659 (1995).
53. Scalia R, Appel JZ 3rd, Lefer AM: Leukocyte-endothelial interaction during the early stages of hypercholesterolemia in the rabbit:-role of P-selectin, ICAM-1, and VCAM-1: Arterioscler. Thromb. Vasc. Biol. 18, 1093-1100 (1998).
54. Hasdai D, Nielson MF, Rizza RA et al.: Attenuated in vitro coronary arteriolar vasorelaxation to insulin-like growth factor I in experimental hypercholesterolemia. Hypertension 34, 89-95 (1999).
55. Stokes KY, Clanton EC, Russell JM, Ross CR, Granger DN: NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte- endothelial cell adhesion. Circ. Res. 88, 499-505 (2001).
56. Ohara Y, Peterson TE, Harrison DG: Hypercholesterolemia increases endothelial superoxide anion production. J. Clin. Invest. 91, 2546-2551 (1993).
57. Chen H, Karne RJ, Hall G et al.: High-dose oral vitamin C partially replenishes vitamin C levels but does not improve endothelial dysfunction or insulin resistance. Am. J. Physiol. Heart Circ. Physiol. 290, H137-H145 (2006).
58. Su J, Lucchesi PA, Gonzalez-Villalobos RA et al.: Role of advance glycation end products with oxidative stress in resistance artery dysfunction in type 2 diabetic mice. Arterioscler. Thromb. Vasc. Biol. 28, 1432-1438 (2008).
59. Paravidni TM, Touyz RM: NADPH oxidases, reactive oxygen species, and hypertension. Diabetes Care 31, S170-S180 (2008).
60. Germanò G, Sanguigni V, Pignatelli P et al.: Enhanced platelet release of superoxide anion in systemic hypertension: role of AT1 receptors. J. Hypertens. 22, 1151-1156 (2004).
61. Touyz RM, Schiffrin EL: Increased generation of superoxide by angiotensin II in smooth muscle cells from resistance arteries of hypertensive patients: role of phospholipase D-dependent NAD(P)H oxidase-sensitive pathways. J. Hypertens. 19, 1245-1254 (2001).
62. Touyz RM, Yao G, Quinn MT, Pagano PJ, Schiffrin EL: p47phox associates with the cytoskeleton through cortactin in human vascular smooth muscle cells: role in NAD(P)H oxidase regulation by angiotensin II. Arterioscler. Thromb. Vasc. Biol. 25, 512-518 (2005).
63. Aggoun Y, Bonnet D, Sidi D et al: Arterial mechanical changes in children with familial hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 20, 2070-2075 (2000).
64. Sorensen KB, Celermajer DS, Georgapoulos D et al.: Impairment of endothelium-dependent dilation is an early event in children with familial hypercholesterolemia and is related to the lipoprotein(a) level. J. Clin. Invest. 93, 50-55 (1994).
65. Celermajer DS, Sorensen KE, Gooch VM et al.: Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet. 340, 1111-1115 (1992).
66. Arcaro G, Zenere BM, Travia D et al.: Non-invasive detection of early endothelial dysfunction in hypercholesterolaemic subjects. Atherosclerosis. 114, 247-254 (1995)
67. Martino F, Loffredo L, Carnevale R et al.: Oxidative stress is associated with arterial dysfunction and enhanced intima - media thickness in children with hypercholesterolemia: the potential role of reduced nicotinamide-adenine dinicleotide phosphate oxidase. Pediatrics 122, E1-E8 (2008).
68. Guzik TJ, Mussa S, Gastaldi D et al.: Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105, 1656-1662 (2002).
69. Rubo SH, Rector TS, Bank AJ, Williams RE, Heifetz SM: Endothelium-dependent vasodilation is attenuated in patients with heart failure. Circulation 34, 1589-1596 (1991).
70. Drexler H, Hayoz D, Münzel T, Just H, Zelis R, Brunner HR: Endothelial function in congestive heart failure. Am. Heart J. 126, 761-764 (1993).
71. Dworakowski R, Walker S, Momin A et al.: Reduced nicotinamide adenine dinucleotide phosphate oxidase-derived superoxide and vascular endothelial dysfunction in human heart failure. J. Am. Coll. Cardiol. 51, 1349-1356 (2008).
72. Levine GN, Frei B, Koulouris SN et al.: Ascorbic acid reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation 93, 1107-1113 (1996).
73. Heitzer T, Schlinzig T, Krohn K et al.: Endothelial dysfunction, oxidative stress and risk of cardiovascular events in patients with coronary artery disease. Circulation 104, 2673-2678 (2001).
74. Hornig B, Landmesser U, Kohler C et al.: Comparative effect of ace inhibition and angiotensin II type 1 receptor antagonism on bioavailability of nitric oxide in patients with coronary artery disease: role of superoxide dismutase. Circulation 103, 799-805 (2001).
75. Guzik TJ, West NE, Black E et al.: Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ. Res. 86, E85-E90 (2000).
76. Spiekermann S, Landmesser U, Dikalov S et al.: Electron spin resonance characterization of vascular xanthine and NAD(P)H oxidase activity in patients with coronary artery disease relation to endothelium-dependent vasodilation. Circulation 107, 1383-1389 (2003).
77. Warnholtz A, Nickening G, Schulz E et al.: Increase NADP-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the rennin - angiotensin system. Circulation 99, 2027-2033 (1999).
78. phox in human coronary arteries. Circulation 100, 1494-1498 (1999).
79. Guzik TJ, Sadowski J, Guzik B et al.: Coronary artery superoxide production and Nox isoform expression in human coronary disease. Arterioscler. Thromb. Vasc. Biol. 26, 333-333 (2006).
80. Jay DB, Papaharalambus CA, Seidel-Rogol B, Dikalova AE, Lassègue B, Griendling KK: Nox5 mediated PDGF-induced proliferation in human aortic smooth muscle cells. Free Radic. Biol. Med. 45, 329-335 (2008).
81. Kirk EA, Dinauer MC, Rosen H, Chait A, Heinecke JW, LeBoeuf RC: Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 20, 1529-1535 (2000).
82. -/- mice J. Clin. Invest. 108, 1513-1522 (2001).
83. Madamanchi NR, Hakim ZS, Runge MS: Oxidative stress in atherogenesis and arterial thrombosis: the disconnect between cellular studies and clinical outcomes. J. Thromb. Haemost. 3, 254-367 (2005).
84. Vendrov AE, Hakim ZS, Madamanchi NR, Rojas M, Madamanchi C, Runge MS: Macrophages and vessel wall cells atherosclerosis is attenuated by limiting superoxide generation in both. Arterioscler. Thromb. Vasc. Biol. 27, 2714-2721 (2007).
85. Donato AJ, Eskurza I, Silver AE et al.: Direct evidence of endothelial oxidative stress with aging in humans. Relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-κB. Circ. Res. 100, 1659-1666 (2007).
86. Zalba G, Beloqui O, San Josè G, Moreno MU, Fortuňo A, Diez J: NADPH oxidase-dependent superoxide production is associated with carotid intima - media thickness in subjects free of clinical atherosclerotic disease. Arterioscler. Thromb. Vasc. Biol. 25, 1452-1457 (2005).
87. O'Leary DH, Polak JF: Intima - media thickness: a to ol for atherosclerosis imaging and event prediction. Am. J. Cardiol. 90, 18L-21L (2002).
88. Patrono C, FitzGerald GA: Isoprostanes: potential markers of oxidant stress in atherothrombotic disease. Arterioscler. Thromb. Vasc. Biol. 17, 2309-2315 (1997).
89. Arca M, Conti B, Montali A et al.: C242T polymorphism of NADPH oxidase p22phox and recurrence of cardiovascular events in coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 28, 752-757 (2008).
90. Cahilly C, Ballantyne CM, Lim DS, Gotto A, Marian AJ: A variant of p22phox, involved in generation of reactive oxygen species in the vessel wall, is associated with progression of coronary atherosclerosis. Circ. Res. 86, 391-395 (2000).
91. Flammer AJ, Hermann F, Wiesli P et al.: Effect of losartan, compared with atenolol, on endothelial function and oxidative stress in patient with type 2 diabetes and hypertension. J. Hypertens. 25, 785-791 (2007).
92. Mason RP, Walter MF, Jacob RF: Effects of HMG-CoA reductase inhibitors on endothelial function: role of microdomains and oxidative stress. Circulation 109, 1134-1141 (2004).
93. - and systolic blood pressure in mice. Circ. Res. 89, 408-414 (2001).
94. Jacobson GM, Dourron HM, Liu J et al.: Novel NAD(P)H oxidase inhibitor suppresses angioplasty-induced superoxide and neointimal hyperplasia of rat carotid artery. Circ. Res. 92, 637-643 (2003).
95. Williams HC, Griendling KK: NADPH oxidase inhibitors: new antihypertensive agents? J. Cardiovasc. Pharmacol. 50, 9-16 (2007).
96. Sumimoto H: Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. EEBS Journal. 275, 3249-3277 (2008).
97. Kobayashi S, Nojima Y, Shibuya M, Maru Y: Nox1 regulates apoptosis and potentially stimulates branching morphogenesis in sinusoidal endothelial cells. Exp Cell. Res. 300, 455-462 (2004).
98. Ago T, Kitazono T, Kuroda J et al.: NAD(P)H oxidases in rat basilar arterial endothelial cells. Stroke 36, 1040-1046 (2005).
99. Segal AW, Abo A: The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem. Sci. 18, 43-47 (1993).
100. Sorescu D, Somers MJ, Lassegue B, Grant S, Harrison DG, Griendling KK: Electron spin resonance characterization of the NAD(P)H oxidase in vascular smooth muscle cells. Free Radic. Biol. Med. 30, 603-612 (2001).
101. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG: Functional analysis of Nox4 reveals unique characteristics compared with other NADPH oxidases. Cell Signal. 18, 69-82 (2006).
102. Hu T, Ramachandrarao SP, Siva S et al.: Reactive oxygen species production via NADPH oxidase mediates TGF-β induced cytoskeletal alterations in endothelial cells. Am. J. Physiol. Renal Physiol. 289, F816-F825 (2005).
103. Ellmark SH, Dusting GJ, Fui MN, Guzzo-Pernell N, Drummond GR: The contribution of Nox4 to NADPH oxidase activity in mouse vascular smooth muscle. Cardiovasc. Res. 65, 495-504 (2005).
104. 2-dependent arachidonic acid production in adult cardiac fibroblasts. FEBS 579, 2533-2540 (2005).
105. Rey FE, Pagano PJ: The reactive adventitia: fibroblast oxidase in vascular function. Arterioscler. Thromb. Vasc. Biol. 22, 1962-1971 (2002).
106. Banfi B, Tirone F, Durussel I et al.: Mechanism of Ca2 activation of the NADPH oxidase 5 (NOX5). J. Biol Chem. 279, 18583-18591 (2004).
107. Kawahara T, Ritsick D, Cheng G, Lambeth JD: Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J. Biol. Chem. 280, 31859-31869 (2005).