Skip to main content
SpringerLink
Log in

Oxidase Interactions in Cardiovascular Disease

  • Reference work entry
  • First Online:
Systems Biology of Free Radicals and Antioxidants

Abstract

Oxidative stress has been implicated in cardiovascular diseases such as hypertension, atherosclerosis, diabetic vascular complications, ischemic heart disease, and heart failure. Reactive oxygen species (ROS) in cardiovascular system are generated from various enzymatic systems such as NADPH oxidase (NOX), uncoupled nitric oxide synthase (NOS), mitochondria and xanthine oxidase. Interactions among these systems have been intensively investigated for their roles in cardiovascular pathogenesis. The current review discusses up-to-date findings regarding pathophysiologies of each oxidase system, complex crosstalks among different oxidase components, and consequences of these crosstalks in mediating cardiovascular pathogenesis. Better understanding of these mechanisms may promote novel therapeutic strategies to prevent or treat cardiovascular diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 1,999.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 2,999.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, Takada J, Wakisaka M, Ibayashi S, Utsumi H, Iida M (2004) Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109:227–233

    CAS  PubMed  Google Scholar 

  • Ahluwalia J (2008) Characterisation of electron currents generated by the human neutrophil NADPH oxidase. Biochem Biophys Res Commun 368:656–661

    CAS  PubMed  Google Scholar 

  • Akasaki T, Ohya Y, Kuroda J, Eto K, Abe I, Sumimoto H, Iida M (2006) Increased expression of gp91phox homologues of NAD(P)H oxidase in the aortic media during chronic hypertension: involvement of the renin-angiotensin system. Hypertens Res 29:813–820

    CAS  PubMed  Google Scholar 

  • Alp NJ, McAteer MA, Khoo J, Choudhury RP, Channon KM (2004) Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohydrolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 24:445–450

    CAS  PubMed  Google Scholar 

  • Anilkumar N, Weber R, Zhang M, Brewer A, Shah AM (2008) Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28:1347–1354

    CAS  PubMed  Google Scholar 

  • Arroyo CM, Kramer JH, Dickens BF, Weglicki WB (1987) Identification of free radicals in myocardial ischemia/reperfusion by spin trapping with nitrone DMPO. FEBS Lett 221:101–104

    CAS  PubMed  Google Scholar 

  • Azumi H, Inoue N, Takeshita S, Rikitake Y, Kawashima S, Hayashi Y, Itoh H, Yokoyama M (1999) Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation 100:1494–1498

    CAS  PubMed  Google Scholar 

  • Bagi Z, Koller A (2003) Lack of nitric oxide mediation of flow-dependent arteriolar dilation in type I diabetes is restored by sepiapterin. J Vasc Res 40:47–57

    CAS  PubMed  Google Scholar 

  • Banfi B, Clark RA, Steger K, Krause KH (2003) Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem 278:3510–3513

    CAS  PubMed  Google Scholar 

  • Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS (2001) p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest 108:1513–1522

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baudry N, Laemmel E, Vicaut E (2008) In vivo reactive oxygen species production induced by ischemia in muscle arterioles of mice: involvement of xanthine oxidase and mitochondria. Am J Physiol Heart Circ Physiol 294:H821–H828

    CAS  PubMed  Google Scholar 

  • Bauersachs J, Bouloumie A, Fraccarollo D, Hu K, Busse R, Ertl G (1998) Hydralazine prevents endothelial dysfunction, but not the increase in superoxide production in nitric oxide-deficient hypertension. Eur J Pharmacol 362:77–81

    CAS  PubMed  Google Scholar 

  • Becker BF (1993) Towards the physiological function of uric acid. Free Radic Biol Med 14:615–631

    CAS  PubMed  Google Scholar 

  • Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313

    CAS  PubMed  Google Scholar 

  • BelAiba RS, Djordjevic T, Petry A, Diemer K, Bonello S, Banfi B, Hess J, Pogrebniak A, Bickel C, Gorlach A (2007) NOX5 variants are functionally active in endothelial cells. Free Radic Biol Med 42:446–459

    CAS  PubMed  Google Scholar 

  • Beswick RA, Dorrance AM, Leite R, Webb RC (2001) NADH/NADPH oxidase and enhanced superoxide production in the mineralocorticoid hypertensive rat. Hypertension 38:1107–1111

    CAS  PubMed  Google Scholar 

  • Bitar MS, Wahid S, Mustafa S, Al-Saleh E, Dhaunsi GS, Al-Mulla F (2005) Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes. Eur J Pharmacol 511:53–64

    CAS  PubMed  Google Scholar 

  • Bolli R, Patel BS, Jeroudi MO, Lai EK, McCay PB (1988) Demonstration of free radical generation in “stunned” myocardium of intact dogs with the use of the spin trap alpha-phenyl N-tert-butyl nitrone. J Clin Invest 82:476–485

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boveris A (1984) Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria. Methods Enzymol 105:429–435

    CAS  PubMed  Google Scholar 

  • Brown JM, Terada LS, Grosso MA, Whitmann GJ, Velasco SE, Patt A, Harken AH, Repine JE (1988) Xanthine oxidase produces hydrogen peroxide which contributes to reperfusion injury of ischemic, isolated, perfused rat hearts. J Clin Invest 81:1297–1301

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230

    CAS  PubMed  Google Scholar 

  • Cadenas E, Boveris A, Ragan CI, Stoppani AO (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180:248–257

    CAS  PubMed  Google Scholar 

  • Cai H (2005) Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc Res 68:26–36

    CAS  PubMed  Google Scholar 

  • Cai H, Harrison DG (2000) Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87:840–844

    CAS  PubMed  Google Scholar 

  • Cai H, Li Z, Goette A, Mera F, Honeycutt C, Feterik K, Wilcox JN, Dudley SC Jr, Harrison DG, Langberg JJ (2002) Downregulation of endocardial nitric oxide synthase expression and nitric oxide production in atrial fibrillation: potential mechanisms for atrial thrombosis and stroke. Circulation 106:2854–2858

    CAS  PubMed  Google Scholar 

  • Cai H, Griendling KK, Harrison DG (2003a) The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 24:471–478

    CAS  PubMed  Google Scholar 

  • Cai H, Li Z, Davis ME, Kanner W, Harrison DG, Dudley SC Jr (2003b) Akt-dependent phosphorylation of serine 1179 and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase 1/2 cooperatively mediate activation of the endothelial nitric-oxide synthase by hydrogen peroxide. Mol Pharmacol 63:325–331

    CAS  PubMed  Google Scholar 

  • Cappola TP, Kass DA, Nelson GS, Berger RD, Rosas GO, Kobeissi ZA, Marban E, Hare JM (2001) Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104:2407–2411

    CAS  PubMed  Google Scholar 

  • Ceylan-Isik AF, Guo KK, Carlson EC, Privratsky JR, Liao SJ, Cai L, Chen AF, Ren J (2009) Metallothionein abrogates GTP cyclohydrolase I inhibition-induced cardiac contractile and morphological defects: role of mitochondrial biogenesis. Hypertension 53:1023–1031

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chalupsky K, Cai H (2005) Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 102:9056–9061

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chamseddine AH, Miller FJ Jr (2003) gp91phox contributes to NADPH oxidase activity in aortic fibroblasts but not smooth muscle cells. Am J Physiol Heart Circ Physiol 285:H2284–H2289

    CAS  PubMed  Google Scholar 

  • Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217:409–427

    CAS  PubMed  Google Scholar 

  • Chen XL, Zhang Q, Zhao R, Ding X, Tummala PE, Medford RM (2003) Rac1 and superoxide are required for the expression of cell adhesion molecules induced by tumor necrosis factor-alpha in endothelial cells. J Pharmacol Exp Ther 305:573–580

    CAS  PubMed  Google Scholar 

  • Cheng G, Lambeth JD (2004) NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J Biol Chem 279:4737–4742

    CAS  PubMed  Google Scholar 

  • Chew GT, Watts GF (2004) Coenzyme Q10 and diabetic endotheliopathy: oxidative stress and the “recoupling hypothesis”. QJM 97:537–548

    CAS  PubMed  Google Scholar 

  • Choi K, Kim J, Kim GW, Choi C (2009) Oxidative stress-induced necrotic cell death via mitochondira-dependent burst of reactive oxygen species. Curr Neurovasc Res 6:213–222

    CAS  PubMed  Google Scholar 

  • Christen S, Bifrare YD, Siegenthaler C, Leib SL, Tauber MG (2001) Marked elevation in cortical urate and xanthine oxidoreductase activity in experimental bacterial meningitis. Brain Res 900:244–251

    CAS  PubMed  Google Scholar 

  • Cifuentes ME, Rey FE, Carretero OA, Pagano PJ (2000) Upregulation of p67(phox) and gp91(phox) in aortas from angiotensin II-infused mice. Am J Physiol Heart Circ Physiol 279:H2234–H2240

    CAS  PubMed  Google Scholar 

  • Clempus RE, Sorescu D, Dikalova AE, Pounkova L, Jo P, Sorescu GP, Schmidt HH, Lassegue B, Griendling KK (2007) Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 27:42–48

    CAS  PubMed Central  PubMed  Google Scholar 

  • Coetzee A, Roussouw G, Macgregor L (1996) Failure of allopurinol to improve left ventricular stroke work after cardiopulmonary bypass surgery. J Cardiothorac Vasc Anesth 10:627–633

    CAS  PubMed  Google Scholar 

  • Coghlan JG, Flitter WD, Clutton SM, Panda R, Daly R, Wright G, Ilsley CD, Slater TF (1994) Allopurinol pretreatment improves postoperative recovery and reduces lipid peroxidation in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 107:248–256

    CAS  PubMed  Google Scholar 

  • Cohn JN, Ferrari R, Sharpe N (2000) Cardiac remodeling–concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an international forum on cardiac remodeling. J Am Coll Cardiol 35:569–582

    CAS  PubMed  Google Scholar 

  • Costa AD, Quinlan CL, Andrukhiv A, West IC, Jaburek M, Garlid KD (2006) The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am J Physiol Heart Circ Physiol 290:H406–H415

    CAS  PubMed  Google Scholar 

  • Crabtree MJ, Channon KM (2011) Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide 25:81–88

    CAS  PubMed  Google Scholar 

  • Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, Keaney JF Jr (2011) NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 124:731–740

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341(Pt 2):233–249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Datla SR, Griendling KK (2010) Reactive oxygen species, NADPH oxidases, and hypertension. Hypertension 56:325–330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dhaunsi GS, Kaur J, Alsaeid K, Turner RB, Bitar MS (2005) Very long chain fatty acids activate NADPH oxidase in human dermal fibroblasts. Cell Biochem Funct 23:65–68

    CAS  PubMed  Google Scholar 

  • Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, Courtneidge SA (2009) Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2:ra53

    PubMed Central  PubMed  Google Scholar 

  • Dikalova A, Clempus R, Lassegue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D, Taylor WR, Schmidt HH, Owens GK, Lambeth JD, Griendling KK (2005) Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112:2668–2676

    CAS  PubMed  Google Scholar 

  • Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI (2010) Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 107:106–116

    CAS  PubMed Central  PubMed  Google Scholar 

  • Doughan AK, Harrison DG, Dikalov SI (2008) Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102:488–496

    CAS  PubMed  Google Scholar 

  • Douglas G, Bendall JK, Crabtree MJ, Tatham AL, Carter EE, Hale AB, Channon KM (2012) Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE(-)/(-) mice. Cardiovasc Res 94:20–29

    CAS  PubMed Central  PubMed  Google Scholar 

  • Druhan LJ, Forbes SP, Pope AJ, Chen CA, Zweier JL, Cardounel AJ (2008) Regulation of eNOS-derived superoxide by endogenous methylarginines. Biochemistry 47:7256–7263

    CAS  PubMed  Google Scholar 

  • Du YH, Guan YY, Alp NJ, Channon KM, Chen AF (2008) Endothelium-specific GTP cyclohydrolase I overexpression attenuates blood pressure progression in salt-sensitive low-renin hypertension. Circulation 117:1045–1054

    CAS  PubMed  Google Scholar 

  • Dworakowski R, Alom-Ruiz SP, Shah AM (2008) NADPH oxidase-derived reactive oxygen species in the regulation of endothelial phenotype. Pharmacol Rep 60:21–28

    CAS  PubMed  Google Scholar 

  • Eltzschig HK, Collard CD (2004) Vascular ischaemia and reperfusion injury. Br Med Bull 70:71–86

    CAS  PubMed  Google Scholar 

  • Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O’Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133:462–474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ferdinandy P, Panas D, Schulz R (1999) Peroxynitrite contributes to spontaneous loss of cardiac efficiency in isolated working rat hearts. Am J Physiol 276:H1861–H1867

    CAS  PubMed  Google Scholar 

  • Fu X, Beer DG, Behar J, Wands J, Lambeth D, Cao W (2006) cAMP-response element-binding protein mediates acid-induced NADPH oxidase NOX5-S expression in Barrett esophageal adenocarcinoma cells. J Biol Chem 281:20368–20382

    CAS  PubMed  Google Scholar 

  • Fukui T, Ishizaka N, Rajagopalan S, Laursen JB, Capers QT, Taylor WR, Harrison DG, de Leon H, Wilcox JN, Griendling KK (1997) p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ Res 80:45–51

    CAS  PubMed  Google Scholar 

  • Gao L, Chalupsky K, Stefani E, Cai H (2009) Mechanistic insights into folic acid-dependent vascular protection: dihydrofolate reductase (DHFR)-mediated reduction in oxidant stress in endothelial cells and angiotensin II-infused mice: a novel HPLC-based fluorescent assay for DHFR activity. J Mol Cell Cardiol 47:752–760

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gao L, Siu KL, Chalupsky K, Nguyen A, Chen P, Weintraub NL, Galis Z, Cai H (2012) Role of uncoupled endothelial nitric oxide synthase in abdominal aortic aneurysm formation: treatment with folic acid. Hypertension 59:158–166

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garlick PB, Davies MJ, Hearse DJ, Slater TF (1987) Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res 61:757–760

    CAS  PubMed  Google Scholar 

  • Gavazzi G, Banfi B, Deffert C, Fiette L, Schappi M, Herrmann F, Krause KH (2006) Decreased blood pressure in NOX1-deficient mice. FEBS Lett 580:497–504

    CAS  PubMed  Google Scholar 

  • Gavin AD, Struthers AD (2005) Allopurinol reduces B-type natriuretic peptide concentrations and haemoglobin but does not alter exercise capacity in chronic heart failure. Heart 91:749–753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gertzberg N, Neumann P, Rizzo V, Johnson A (2004) NAD(P)H oxidase mediates the endothelial barrier dysfunction induced by TNF-alpha. Am J Physiol Lung Cell Mol Physiol 286:L37–L48

    CAS  PubMed  Google Scholar 

  • Giardino I, Edelstein D, Brownlee M (1996) BCL-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells. J Clin Invest 97:1422–1428

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gimpel JA, Lahpor JR, van der Molen AJ, Damen J, Hitchcock JF (1995) Reduction of reperfusion injury of human myocardium by allopurinol: a clinical study. Free Radic Biol Med 19:251–255

    CAS  PubMed  Google Scholar 

  • Gladden JD, Zelickson BR, Wei CC, Ulasova E, Zheng J, Ahmed MI, Chen Y, Bamman M, Ballinger S, Darley-Usmar V, Dell’Italia LJ (2011) Novel insights into interactions between mitochondria and xanthine oxidase in acute cardiac volume overload. Free Radic Biol Med 51:1975–1984

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gokce N, Holbrook M, Duffy SJ, Demissie S, Cupples LA, Biegelsen E, Keaney JF Jr, Loscalzo J, Vita JA (2001) Effects of race and hypertension on flow-mediated and nitroglycerin-mediated dilation of the brachial artery. Hypertension 38:1349–1354

    CAS  PubMed  Google Scholar 

  • Gray SP, Di Marco E, Okabe J, Szyndralewiez C, Heitz F, Montezano AC, de Haan JB, Koulis C, El-Osta A, Andrews KL, Chin-Dusting JP, Touyz RM, Wingler K, Cooper ME, Schmidt HH, Jandeleit-Dahm KA (2012) NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 127:1888–1902

    Google Scholar 

  • Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74:1141–1148

    CAS  PubMed  Google Scholar 

  • Groemping Y, Lapouge K, Smerdon SJ, Rittinger K (2003) Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113:343–355

    CAS  PubMed  Google Scholar 

  • Guan W, Osanai T, Kamada T, Hanada H, Ishizaka H, Onodera H, Iwasa A, Fujita N, Kudo S, Ohkubo T, Okumura K (2003) Effect of allopurinol pretreatment on free radical generation after primary coronary angioplasty for acute myocardial infarction. J Cardiovasc Pharmacol 41:699–705

    CAS  PubMed  Google Scholar 

  • Gupte SA, Kaminski PM, George S, Kouznestova L, Olson SC, Mathew R, Hintze TH, Wolin MS (2009) Peroxide generation by p47phox-Src activation of Nox2 has a key role in protein kinase C-induced arterial smooth muscle contraction. Am J Physiol Heart Circ Physiol 296:H1048–H1057

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guzik TJ, West NE, Black E, McDonald D, Ratnatunga C, Pillai R, Channon KM (2000) Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res 86:E85–E90

    CAS  PubMed  Google Scholar 

  • Guzik TJ, Chen W, Gongora MC, Guzik B, Lob HE, Mangalat D, Hoch N, Dikalov S, Rudzinski P, Kapelak B, Sadowski J, Harrison DG (2008) Calcium-dependent NOX5 nicotinamide adenine dinucleotide phosphate oxidase contributes to vascular oxidative stress in human coronary artery disease. J Am Coll Cardiol 52:1803–1809

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn NE, Meischl C, Wijnker PJ, Musters RJ, Fornerod M, Janssen HW, Paulus WJ, van Rossum AC, Niessen HW, Krijnen PA (2011) NOX2, p22phox and p47phox are targeted to the nuclear pore complex in ischemic cardiomyocytes colocalizing with local reactive oxygen species. Cell Physiol Biochem 27:471–478

    CAS  PubMed  Google Scholar 

  • Hahn NE, Meischl C, Kawahara T, Musters RJ, Verhoef VM, van der Velden J, Vonk AB, Paulus WJ, van Rossum AC, Niessen HW, Krijnen PA (2012) NOX5 expression is increased in intramyocardial blood vessels and cardiomyocytes after acute myocardial infarction in humans. Am J Pathol 180:2222–2229

    CAS  PubMed  Google Scholar 

  • Han D, Williams E, Cadenas E (2001) Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem J 353:411–416

    CAS  PubMed Central  PubMed  Google Scholar 

  • Han D, Antunes F, Canali R, Rettori D, Cadenas E (2003) Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278:5557–5563

    CAS  PubMed  Google Scholar 

  • Hanna IR, Hilenski LL, Dikalova A, Taniyama Y, Dikalov S, Lyle A, Quinn MT, Lassegue B, Griendling KK (2004) Functional association of nox1 with p22phox in vascular smooth muscle cells. Free Radic Biol Med 37:1542–1549

    CAS  PubMed  Google Scholar 

  • Harrison R (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33:774–797

    CAS  PubMed  Google Scholar 

  • Harrison DG, Gongora MC, Guzik TJ, Widder J (2007) Oxidative stress and hypertension. J Am Soc Hypertens 1:30–44

    PubMed  Google Scholar 

  • Hattori Y, Nakanishi N, Akimoto K, Yoshida M, Kasai K (2003) HMG-CoA reductase inhibitor increases GTP cyclohydrolase I mRNA and tetrahydrobiopterin in vascular endothelial cells. Arterioscler Thromb Vasc Biol 23:176–182

    CAS  PubMed  Google Scholar 

  • Heitzer T, Wenzel U, Hink U, Krollner D, Skatchkov M, Stahl RA, MacHarzina R, Brasen JH, Meinertz T, Munzel T (1999) Increased NAD(P)H oxidase-mediated superoxide production in renovascular hypertension: evidence for an involvement of protein kinase C. Kidney Int 55:252–260

    CAS  PubMed  Google Scholar 

  • Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G, Shah AM (2003) Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41:2164–2171

    CAS  PubMed  Google Scholar 

  • Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24:677–683

    CAS  PubMed  Google Scholar 

  • Hille R, Nishino T (1995) Flavoprotein structure and mechanism. 4. Xanthine oxidase and xanthine dehydrogenase. Faseb J 9:995–1003

    CAS  PubMed  Google Scholar 

  • 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 (2001) Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88:E14–E22

    CAS  PubMed  Google Scholar 

  • Hwang J, Saha A, Boo YC, Sorescu GP, McNally JS, Holland SM, Dikalov S, Giddens DP, Griendling KK, Harrison DG, Jo H (2003) Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem 278:47291–47298. Epub 42003 Sep 47294

    CAS  PubMed  Google Scholar 

  • Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, Uchida K, Arimura K, Egashira K, Takeshita A (1999) Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 85:357–363

    CAS  PubMed  Google Scholar 

  • Ide T, Tsutsui H, Kinugawa S, Suematsu N, Hayashidani S, Ichikawa K, Utsumi H, Machida Y, Egashira K, Takeshita A (2000) Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res 86:152–157

    CAS  PubMed  Google Scholar 

  • Inoguchi T, Sonta T, Tsubouchi H, Etoh T, Kakimoto M, Sonoda N, Sato N, Sekiguchi N, Kobayashi K, Sumimoto H, Utsumi H, Nawata H (2003) Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase. J Am Soc Nephrol 14:S227–S232

    CAS  PubMed  Google Scholar 

  • Jay DB, Papaharalambus CA, Seidel-Rogol B, Dikalova AE, Lassegue B, Griendling KK (2008) Nox5 mediates PDGF-induced proliferation in human aortic smooth muscle cells. Free Radic Biol Med 45:329–335

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson FK, Johnson RA, Peyton KJ, Durante W (2005) Arginase inhibition restores arteriolar endothelial function in Dahl rats with salt-induced hypertension. Am J Physiol Regul Integr Comp Physiol 288:R1057–R1062

    CAS  PubMed  Google Scholar 

  • Judkins CP, Diep H, Broughton BR, Mast AE, Hooker EU, Miller AA, Selemidis S, Dusting GJ, Sobey CG, Drummond GR (2010) Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE-/- mice. Am J Physiol Heart Circ Physiol 298:H24–H32

    CAS  PubMed  Google Scholar 

  • Jung O, Schreiber JG, Geiger H, Pedrazzini T, Busse R, Brandes RP (2004) gp91phox-containing NADPH oxidase mediates endothelial dysfunction in renovascular hypertension. Circulation 109:1795–1801

    CAS  PubMed  Google Scholar 

  • Kim YM, Guzik TJ, Zhang YH, Zhang MH, Kattach H, Ratnatunga C, Pillai R, Channon KM, Casadei B (2005) A myocardial Nox2 containing NAD(P)H oxidase contributes to oxidative stress in human atrial fibrillation. Circ Res 97:629–636

    CAS  PubMed  Google Scholar 

  • Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, Suzuki T, Maeta H, Abe Y (2005) Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 45:860–866

    CAS  PubMed  Google Scholar 

  • Kirk EA, Dinauer MC, Rosen H, Chait A, Heinecke JW, LeBoeuf RC (2000) Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice. Arterioscler Thromb Vasc Biol 20:1529–1535

    CAS  PubMed  Google Scholar 

  • Kobori H, Nishiyama A (2004) Effects of tempol on renal angiotensinogen production in Dahl salt-sensitive rats. Biochem Biophys Res Commun 315:746–750

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kowluru RA, Abbas SN (2003) Diabetes-induced mitochondrial dysfunction in the retina. Invest Ophthalmol Vis Sci 44:5327–5334

    PubMed  Google Scholar 

  • Krijnen PA, Meischl C, Hack CE, Meijer CJ, Visser CA, Roos D, Niessen HW (2003) Increased Nox2 expression in human cardiomyocytes after acute myocardial infarction. J Clin Pathol 56:194–199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuroda J, Nakagawa K, Yamasaki T, Nakamura K, Takeya R, Kuribayashi F, Imajoh-Ohmi S, Igarashi K, Shibata Y, Sueishi K, Sumimoto H (2005) The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells 10:1139–1151

    CAS  PubMed  Google Scholar 

  • Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J (2010) NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 107:15565–15570

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kutala VK, Khan M, Angelos MG, Kuppusamy P (2007) Role of oxygen in postischemic myocardial injury. Antioxid Redox Signal 9:1193–1206

    CAS  PubMed  Google Scholar 

  • Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181–189

    CAS  PubMed  Google Scholar 

  • Landmesser U, Drexler H (2002) Allopurinol and endothelial function in heart failure: future or fantasy? Circulation 106:173–175

    PubMed  Google Scholar 

  • Landmesser U, Cai H, Dikalov S, McCann L, Hwang J, Jo H, Holland SM, Harrison DG (2002) Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40:511–515

    CAS  PubMed  Google Scholar 

  • Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111:1201–1209

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lassegue B, Griendling KK (2010) NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 30:653–661

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK (2001) 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

    CAS  PubMed  Google Scholar 

  • Li JM, Shah AM (2002) Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J Biol Chem 277:19952–19960

    CAS  PubMed  Google Scholar 

  • Li Q, Zhang Y, Marden JJ, Banfi B, Engelhardt JF (2008) Endosomal NADPH oxidase regulates c-Src activation following hypoxia/reoxygenation injury. Biochem J 411:531–541

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li L, Chen W, Rezvan A, Jo H, Harrison DG (2011) Tetrahydrobiopterin deficiency and nitric oxide synthase uncoupling contribute to atherosclerosis induced by disturbed flow. Arterioscler Thromb Vasc Biol 31:1547–1554

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu S, Ma X, Gong M, Shi L, Lincoln T, Wang S (2007) Glucose down-regulation of cGMP-dependent protein kinase I expression in vascular smooth muscle cells involves NAD(P)H oxidase-derived reactive oxygen species. Free Radic Biol Med 42:852–863

    PubMed  Google Scholar 

  • Lob HE, Schultz D, Marvar PJ, Davisson RL, Harrison DG (2013) Role of the NADPH oxidases in the subfornical organ in angiotensin II-induced hypertension. Hypertension 61(2):382–7

    Google Scholar 

  • Loffredo L, Martino F, Carnevale R, Pignatelli P, Catasca E, Perri L, Calabrese CM, Palumbo MM, Baratta F, Del Ben M, Angelico F, Violi F (2012) Obesity and hypercholesterolemia are associated with NOX2 generated oxidative stress and arterial dysfunction. J Pediatr 161(6):1004–1009

    CAS  PubMed  Google Scholar 

  • Loor G, Kondapalli J, Iwase H, Chandel NS, Waypa GB, Guzy RD, Vanden Hoek TL, Schumacker PT (2011) Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim Biophys Acta 1813:1382–1394

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lyle AN, Deshpande NN, Taniyama Y, Seidel-Rogol B, Pounkova L, Du P, Papaharalambus C, Lassegue B, Griendling KK (2009) Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res 105:249–259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Macfarlane DP, Paterson KR, Fisher M (2007) Oral antidiabetic agents as cardiovascular drugs. Diabetes Obes Metab 9:23–30

    CAS  PubMed  Google Scholar 

  • Manea A, Raicu M, Simionescu M (2005) Expression of functionally phagocyte-type NAD(P)H oxidase in pericytes: effect of angiotensin II and high glucose. Biol Cell 97:723–734

    CAS  PubMed  Google Scholar 

  • Mariappan N, Elks CM, Sriramula S, Guggilam A, Liu Z, Borkhsenious O, Francis J (2010) NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 85:473–483

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG (2006) Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18:69–82

    CAS  PubMed  Google Scholar 

  • Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H, Yabe-Nishimura C (2005) Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112:2677–2685

    CAS  PubMed  Google Scholar 

  • Maxwell SR, Lip GY (1997) Reperfusion injury: a review of the pathophysiology, clinical manifestations and therapeutic options. Int J Cardiol 58:95–117

    CAS  PubMed  Google Scholar 

  • Mayhan WG, Arrick DM, Sharpe GM, Patel KP, Sun H (2006) Inhibition of NAD(P)H oxidase alleviates impaired NOS-dependent responses of pial arterioles in type 1 diabetes mellitus. Microcirculation 13:567–575

    CAS  PubMed  Google Scholar 

  • Mazzali M, Hughes J, Kim YG, Jefferson JA, Kang DH, Gordon KL, Lan HY, Kivlighn S, Johnson RJ (2001) Elevated uric acid increases blood pressure in the rat by a novel crystal-independent mechanism. Hypertension 38:1101–1106

    CAS  PubMed  Google Scholar 

  • Meneshian A, Bulkley GB (2002) The physiology of endothelial xanthine oxidase: from urate catabolism to reperfusion injury to inflammatory signal transduction. Microcirculation 9:161–175

    CAS  PubMed  Google Scholar 

  • Miller FJ Jr, Filali M, Huss GJ, Stanic B, Chamseddine A, Barna TJ, Lamb FS (2007) Cytokine activation of nuclear factor kappa B in vascular smooth muscle cells requires signaling endosomes containing Nox1 and ClC-3. Circ Res 101:663–671

    CAS  PubMed  Google Scholar 

  • Ming XF, Barandier C, Viswambharan H, Kwak BR, Mach F, Mazzolai L, Hayoz D, Ruffieux J, Rusconi S, Montani JP, Yang Z (2004) Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation 110:3708–3714

    CAS  PubMed  Google Scholar 

  • Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD (2003) Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92:e31–e40

    CAS  PubMed  Google Scholar 

  • Mollnau H, Wendt M, Szocs K, Lassegue B, Schulz E, Oelze M, Li H, Bodenschatz M, August M, Kleschyov AL, Tsilimingas N, Walter U, Forstermann U, Meinertz T, Griendling K, Munzel T (2002) Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ Res 90:E58–E65

    PubMed  Google Scholar 

  • Monteiro P, Duarte AI, Goncalves LM, Providencia LA (2005) Valsartan improves mitochondrial function in hearts submitted to acute ischemia. Eur J Pharmacol 518:158–164

    CAS  PubMed  Google Scholar 

  • Montezano AC, Burger D, Paravicini TM, Chignalia AZ, Yusuf H, Almasri M, He Y, Callera GE, He G, Krause KH, Lambeth D, Quinn MT, Touyz RM (2010) Nicotinamide adenine dinucleotide phosphate reduced oxidase 5 (Nox5) regulation by angiotensin II and endothelin-1 is mediated via calcium/calmodulin-dependent, rac-1-independent pathways in human endothelial cells. Circ Res 106:1363–1373

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murdoch CE, Alom-Ruiz SP, Wang M, Zhang M, Walker S, Yu B, Brewer A, Shah AM (2011) Role of endothelial Nox2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res Cardiol 106:527–538

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagler RM, Klein I, Zarzhevsky N, Drigues N, Reznick AZ (2002) Characterization of the differentiated antioxidant profile of human saliva. Free Radic Biol Med 32:268–277

    CAS  PubMed  Google Scholar 

  • Nakazono K, Watanabe N, Matsuno K, Sasaki J, Sato T, Inoue M (1991) Does superoxide underlie the pathogenesis of hypertension? Proc Natl Acad Sci USA 88:10045–10048

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H (2009) Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 297:H1535–H1543

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787–790

    CAS  PubMed  Google Scholar 

  • Nishino T (1994) The conversion of xanthine dehydrogenase to xanthine oxidase and the role of the enzyme in reperfusion injury. J Biochem 116:1–6

    CAS  PubMed  Google Scholar 

  • Oak JH, Cai H (2007) Attenuation of angiotensin II signaling recouples eNOS and inhibits nonendothelial NOX activity in diabetic mice. Diabetes 56:118–126

    CAS  PubMed  Google Scholar 

  • Ohashi M, Runge MS, Faraci FM, Heistad DD (2006) MnSOD deficiency increases endothelial dysfunction in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 26:2331–2336

    CAS  PubMed  Google Scholar 

  • Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT (1997) Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc Natl Acad Sci USA 94:14483–14488

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM (2000) Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ Res 87:460–466

    CAS  PubMed  Google Scholar 

  • Park Y, Yang J, Zhang H, Chen X, Zhang C (2011) Effect of PAR2 in regulating TNF-alpha and NAD(P)H oxidase in coronary arterioles in type 2 diabetic mice. Basic Res Cardiol 106:111–123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Parmley LF, Mufti AG, Downey JM (1992) Allopurinol therapy of ischemic heart disease with infarct extension. Can J Cardiol 8:280–286

    CAS  PubMed  Google Scholar 

  • Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, Prunet C, Marie JC, Pouzet C, Samadi M, Elbim C, O’Dowd Y, Bens M, Vandewalle A, Gougerot-Pocidalo MA, Lizard G, Ogier-Denis E (2004) NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol 24:10703–10717

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perrelli MG, Pagliaro P, Penna C (2011) Ischemia/reperfusion injury and cardioprotective mechanisms: Role of mitochondria and reactive oxygen species. World J Cardiol 3:186–200

    PubMed Central  PubMed  Google Scholar 

  • Peshavariya H, Dusting GJ, Jiang F, Halmos LR, Sobey CG, Drummond GR, Selemidis S (2009) NADPH oxidase isoform selective regulation of endothelial cell proliferation and survival. Naunyn Schmiedebergs Arch Pharmacol 380:193–204

    CAS  PubMed  Google Scholar 

  • Peterson JR, Burmeister MA, Tian X, Zhou Y, Guruju MR, Stupinski JA, Sharma RV, Davisson RL (2009) Genetic silencing of Nox2 and Nox4 reveals differential roles of these NADPH oxidase homologues in the vasopressor and dipsogenic effects of brain angiotensin II. Hypertension 54:1106–1114

    CAS  PubMed Central  PubMed  Google Scholar 

  • Petry A, Djordjevic T, Weitnauer M, Kietzmann T, Hess J, Gorlach A (2006) NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxid Redox Signal 8:1473–1484

    CAS  PubMed  Google Scholar 

  • Powell CS, Jackson RM (2003) Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: modulation of enzyme activities by MnSOD. Am J Physiol Lung Cell Mol Physiol 285:L189–L198

    CAS  PubMed  Google Scholar 

  • Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG (1996) 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, Wang YX (2008) Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med 45:1223–1231

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom-Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, Shah AM (2011) Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol 31:1368–1376

    CAS  PubMed  Google Scholar 

  • Romero MJ, Platt DH, Tawfik HE, Labazi M, El-Remessy AB, Bartoli M, Caldwell RB, Caldwell RW (2008) Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ Res 102:95–102

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ryoo S, Lemmon CA, Soucy KG, Gupta G, White AR, Nyhan D, Shoukas A, Romer LH, Berkowitz DE (2006) Oxidized low-density lipoprotein-dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res 99:951–960

    CAS  PubMed  Google Scholar 

  • San Martin A, Foncea R, Laurindo FR, Ebensperger R, Griendling KK, Leighton F (2007) Nox1-based NADPH oxidase-derived superoxide is required for VSMC activation by advanced glycation end-products. Free Radic Biol Med 42:1671–1679

    CAS  PubMed  Google Scholar 

  • Santos CX, Tanaka LY, Wosniak J, Laurindo FR (2009) Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 11:2409–2427

    CAS  PubMed  Google Scholar 

  • Sawyer DB, Colucci WS (2000) Mitochondrial oxidative stress in heart failure: “oxygen wastage” revisited. Circ Res 86:119–120

    CAS  PubMed  Google Scholar 

  • Schroder K, Helmcke I, Palfi K, Krause KH, Busse R, Brandes RP (2007) Nox1 mediates basic fibroblast growth factor-induced migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 27:1736–1743

    PubMed  Google Scholar 

  • Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP (2012) Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 110:1217–1225

    PubMed  Google Scholar 

  • Sheehan AL, Carrell S, Johnson B, Stanic B, Banfi B, Miller FJ Jr (2011) Role for Nox1 NADPH oxidase in atherosclerosis. Atherosclerosis 216:321–326

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sipkens JA, Hahn N, van den Brand CS, Meischl C, Cillessen SA, Smith DE, Juffermans LJ, Musters RJ, Roos D, Jakobs C, Blom HJ, Smulders YM, Krijnen PA, Stehouwer CD, Rauwerda JA, van Hinsbergh VW, Niessen HW (2011) Homocysteine-induced apoptosis in endothelial cells coincides with nuclear NOX2 and peri-nuclear NOX4 activity. Cell Biochem Biophys. doi:10.1007/s12013-011-9297-y

    Google Scholar 

  • Sorescu D, Somers MJ, Lassegue B, Grant S, Harrison DG, Griendling KK (2001) Electron spin resonance characterization of the NAD(P)H oxidase in vascular smooth muscle cells. Free Radic Biol Med 30:603–612

    CAS  PubMed  Google Scholar 

  • Sorescu D, Weiss D, Lassegue B, Clempus RE, Szocs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR, Griendling KK (2002) Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105:1429–1435

    CAS  PubMed  Google Scholar 

  • Spallarossa P, Altieri P, Garibaldi S, Ghigliotti G, Barisione C, Manca V, Fabbi P, Ballestrero A, Brunelli C, Barsotti A (2006) Matrix metalloproteinase-2 and -9 are induced differently by doxorubicin in H9c2 cells: the role of MAP kinases and NAD(P)H oxidase. Cardiovasc Res 69:736–745

    CAS  PubMed  Google Scholar 

  • Stirpe F, Della CE (1969) The regulation of rat liver xanthine oxidase. Conversion in vitro of the enzyme activity from dehydrogenase (type D) to oxidase (type O). J Biol Chem 244:3855–3863

    CAS  PubMed  Google Scholar 

  • Su J, Lucchesi PA, Gonzalez-Villalobos RA, Palen DI, Rezk BM, Suzuki Y, Boulares HA, Matrougui K (2008) Role of advanced glycation end products with oxidative stress in resistance artery dysfunction in type 2 diabetic mice. Arterioscler Thromb Vasc Biol 28:1432–1438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79–82

    CAS  PubMed  Google Scholar 

  • Suzuki H, DeLano FA, Parks DA, Jamshidi N, Granger DN, Ishii H, Suematsu M, Zweifach BW, Schmid-Schonbein GW (1998) Xanthine oxidase activity associated with arterial blood pressure in spontaneously hypertensive rats. Proc Natl Acad Sci USA 95:4754–4759

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swei A, Lacy F, Delano FA, Parks DA, Schmid-Schonbein GW (1999) A mechanism of oxygen free radical production in the Dahl hypertensive rat. Microcirculation 6:179–187

    CAS  PubMed  Google Scholar 

  • Szanto I, Rubbia-Brandt L, Kiss P, Steger K, Banfi B, Kovari E, Herrmann F, Hadengue A, Krause KH (2005) Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol 207:164–176

    CAS  PubMed  Google Scholar 

  • Taggart DP, Young V, Hooper J, Kemp M, Walesby R, Magee P, Wright JE (1994) Lack of cardioprotective efficacy of allopurinol in coronary artery surgery. Br Heart J 71:177–181

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takaya T, Hirata K, Yamashita T, Shinohara M, Sasaki N, Inoue N, Yada T, Goto M, Fukatsu A, Hayashi T, Alp NJ, Channon KM, Yokoyama M, Kawashima S (2007) A specific role for eNOS-derived reactive oxygen species in atherosclerosis progression. Arterioscler Thromb Vasc Biol 27:1632–1637

    CAS  PubMed  Google Scholar 

  • Takimoto E, Kass DA (2007) Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 49:241–248

    CAS  PubMed  Google Scholar 

  • Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, Kass DA (2005) Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115:1221–1231

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas SR, Chen K, Keaney JF Jr (2002) Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 277:6017–6024

    CAS  PubMed  Google Scholar 

  • Thomas M, Gavrila D, McCormick ML, Miller FJ Jr, Daugherty A, Cassis LA, Dellsperger KC, Weintraub NL (2006) Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation 114:404–413

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thony B, Auerbach G, Blau N (2000) Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem J 347(Pt 1):1–16

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW (2005) Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation 111:2347–2355

    CAS  PubMed  Google Scholar 

  • Usui M, Egashira K, Kitamoto S, Koyanagi M, Katoh M, Kataoka C, Shimokawa H, Takeshita A (1999) Pathogenic role of oxidative stress in vascular angiotensin-converting enzyme activation in long-term blockade of nitric oxide synthesis in rats. Hypertension 34:546–551

    CAS  PubMed  Google Scholar 

  • Van Buul JD, Fernandez-Borja M, Anthony EC, Hordijk PL (2005) Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxid Redox Signal 7:308–317

    PubMed  Google Scholar 

  • Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr (1998) Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 95:9220–9225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang HD, Xu S, Johns DG, Du Y, Quinn MT, Cayatte AJ, Cohen RA (2001) Role of NADPH oxidase in the vascular hypertrophic and oxidative stress response to angiotensin II in mice. Circ Res 88:947–953

    CAS  PubMed  Google Scholar 

  • Wang P, Tang F, Li R, Zhang H, Chen S, Liu P, Huang H (2007) Contribution of different Nox homologues to cardiac remodeling in two-kidney two-clip renovascular hypertensive rats: effect of valsartan. Pharmacol Res 55:408–417

    CAS  PubMed  Google Scholar 

  • Watts GF, Playford DA, Croft KD, Ward NC, Mori TA, Burke V (2002) Coenzyme Q(10) improves endothelial dysfunction of the brachial artery in Type II diabetes mellitus. Diabetologia 45:420–426

    CAS  PubMed  Google Scholar 

  • Waud WR, Rajagopalan KV (1976) Purification and properties of the NAD + -dependent (type D) and O2-dependent (type O) forms of rat liver xanthine dehydrogenase. Arch Biochem Biophys 172:354–364

    CAS  PubMed  Google Scholar 

  • Waypa GB, Marks JD, Mack MM, Boriboun C, Mungai PT, Schumacker PT (2002) Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ Res 91:719–726

    CAS  PubMed  Google Scholar 

  • Waypa GB, Guzy R, Mungai PT, Mack MM, Marks JD, Roe MW, Schumacker PT (2006) Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells. Circ Res 99:970–978

    CAS  PubMed  Google Scholar 

  • Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J, Dokic D, Schumacker PT (2010) Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res 106:526–535

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weidemann A, Johnson RS (2008) Biology of HIF-1alpha. Cell Death Differ 15:621–627

    CAS  PubMed  Google Scholar 

  • Werner-Felmayer G, Golderer G, Werner ER (2002) Tetrahydrobiopterin biosynthesis, utilization and pharmacological effects. Curr Drug Metab 3:159–173

    CAS  PubMed  Google Scholar 

  • Wever RM, van Dam T, van Rijn HJ, de Groot F, Rabelink TJ (1997) Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. Biochem Biophys Res Commun 237:340–344

    CAS  PubMed  Google Scholar 

  • Widder JD, Chen W, Li L, Dikalov S, Thony B, Hatakeyama K, Harrison DG (2007) Regulation of tetrahydrobiopterin biosynthesis by shear stress. Circ Res 101:830–838. Epub 2007 Aug 2017

    CAS  PubMed  Google Scholar 

  • Widder JD, Fraccarollo D, Galuppo P, Hansen JM, Jones DP, Ertl G, Bauersachs J (2009) Attenuation of angiotensin II-induced vascular dysfunction and hypertension by overexpression of Thioredoxin 2. Hypertension 54:338–344

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wingler K, Wunsch S, Kreutz R, Rothermund L, Paul M, Schmidt HH (2001) Upregulation of the vascular NAD(P)H-oxidase isoforms Nox1 and Nox4 by the renin-angiotensin system in vitro and in vivo. Free Radic Biol Med 31:1456–1464

    CAS  PubMed  Google Scholar 

  • Wu R, Millette E, Wu L, de Champlain J (2001) Enhanced superoxide anion formation in vascular tissues from spontaneously hypertensive and desoxycorticosterone acetate-salt hypertensive rats. J Hypertens 19:741–748

    CAS  PubMed  Google Scholar 

  • Xia Y, Dawson VL, Dawson TM, Snyder SH, Zweier JL (1996) Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA 93:6770–6774

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu S, He Y, Vokurkova M, Touyz RM (2009) Endothelial cells negatively modulate reactive oxygen species generation in vascular smooth muscle cells: role of thioredoxin. Hypertension 54:427–433

    CAS  PubMed  Google Scholar 

  • Youn JY, Gao L, Cai H (2012a) The p47(phox)- and NADPH oxidase organiser 1 (NOXO1)-dependent activation of NADPH oxidase 1 (NOX1) mediates endothelial nitric oxide synthase (eNOS) uncoupling and endothelial dysfunction in a streptozotocin-induced murine model of diabetes. Diabetologia 55(7):2069–2079

    CAS  PubMed Central  PubMed  Google Scholar 

  • Youn JY, Wang T, Blair J, Laude KM, Oak JH, McCann LA, Harrison DG, Cai HL (2012b) Endothelium-specific sepiapterin reductase deficiency in DOCA-salt hypertension. Am J Physiol Heart Circ Physiol 302(11):H2243–H2249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zalba G, Beaumont FJ, San Jose G, Fortuno A, Fortuno MA, Etayo JC, Diez J (2000) Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension 35:1055–1061

    CAS  PubMed  Google Scholar 

  • Zhang J, Youn JY, Kim AY, Ramirez RJ, Gao L, Ngo D, Chen P, Scovotti J, Mahajan A, Cai H (2012) NOX4-dependent hydrogen peroxide overproduction in human atrial fibrillation and HL-1 atrial cells: relationship to hypertension. Front Physiol 3:140

    PubMed Central  PubMed  Google Scholar 

  • Zheng JS, Yang XQ, Lookingland KJ, Fink GD, Hesslinger C, Kapatos G, Kovesdi I, Chen AF (2003) Gene transfer of human guanosine 5′-triphosphate cyclohydrolase I restores vascular tetrahydrobiopterin level and endothelial function in low renin hypertension. Circulation 108:1238–1245

    CAS  PubMed  Google Scholar 

  • Zimmerman MC, Dunlay RP, Lazartigues E, Zhang Y, Sharma RV, Engelhardt JF, Davisson RL (2004) Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res 95:532–539

    CAS  PubMed  Google Scholar 

  • Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001–1014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zweier JL, Flaherty JT, Weisfeldt ML (1987) Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84:1404–1407

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Divisions of Molecular Medicine and Cardiology, Cardiovascular Research Laboratories, Departments of Anesthesiology and Medicine, Cardiovascular Research Laboratories, David Geffen School of Medicine at University of California Los Angeles, 650 Charles E. Young Drive, Los Angeles, CA, 90095, USA

    Ji Youn Youn, Kin Lung Siu, Qiang Li & Hua Cai

  2. Division of Clinical Pharmacology, Department of Medicine, Vanderbilt University, Nashville, TN

    David G. Harrison

Authors
  1. Ji Youn Youn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kin Lung Siu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David G. Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hua Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hua Cai .

Editor information

Editors and Affiliations

  1. Department of Pharmacology and Therapeutics, University of British Colombia, Vancouver, British Columbia, Canada

    Ismail Laher

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this entry

Cite this entry

Youn, J.Y., Siu, K.L., Li, Q., Harrison, D.G., Cai, H. (2014). Oxidase Interactions in Cardiovascular Disease. In: Laher, I. (eds) Systems Biology of Free Radicals and Antioxidants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30018-9_43

Download citation

Publish with us

Policies and ethics

Search

Navigation