Circulation. 2002;105:1656-1662
Published online before print March 18, 2002, doi: 10.1161/01.CIR.0000012748.58444.08
Published online before print March 18, 2002, doi: 10.1161/01.CIR.0000012748.58444.08
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(Circulation. 2002;105:1656.)
© 2002 American Heart Association, Inc.
Clinical Investigation and Reports |
Mechanisms of Increased Vascular Superoxide Production in Human Diabetes Mellitus
Role of NAD(P)H Oxidase and Endothelial Nitric Oxide Synthase
From the Departments of Cardiovascular Medicine (T.J.G., S.M., K.M.C.) and Cardiothoracic Surgery (S.M., D.G., C.R., R.P.), University of Oxford, Oxford, UK, and Departments of Medicine (T.J.G.) and Cardiovascular Surgery and Transplantology (J.S.), Jagiellonian University School of Medicine, Cracow, Poland.
Correspondence to Dr Keith Channon, MD, MRCP, Department of Cardiovascular Medicine, John Radcliffe Hospital, Oxford OX3 9DU, UK. E-mail keith.channon{at}cardiov.ox.ac.uk
Background— Increased superoxide production contributes to reduced vascular nitric oxide (NO) bioactivity and endothelial dysfunction in experimental models of diabetes. We characterized the sources and mechanisms underlying vascular superoxide production in human blood vessels from diabetic patients with coronary artery disease compared with nondiabetic patients.
Methods and Results— Vascular superoxide production was quantified in both saphenous veins and internal mammary arteries from 45 diabetic and 45 matched nondiabetic patients undergoing coronary artery bypass surgery. NAD(P)H-dependent oxidases were important sources of vascular superoxide in both diabetic and nondiabetic patients, but both the activity of this enzyme system and the levels of NAD(P)H oxidase protein subunits (p22phox, p67phox, and p47phox) were significantly increased in diabetic veins and arteries. In nondiabetic vessels, endothelial NO synthase produced NO that scavenged superoxide. However, in diabetic vessels, the endothelium was an additional net source of superoxide production because of dysfunctional endothelial NO synthase that was corrected by intracellular tetrahydrobiopterin supplementation. Furthermore, increased superoxide production in diabetes was abrogated by the protein kinase C inhibitor chelerythrine.
Conclusions— These observations suggest important roles for NAD(P)H oxidases, endothelial NO synthase uncoupling, and protein kinase C signaling in mediating increased vascular superoxide production and endothelial dysfunction in human diabetes mellitus.
Key Words: diabetes mellitus • atherosclerosis • endothelium • superoxide • nitric oxide
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C. Antoniades, D. Tousoulis, C. Vasiliadou, C. Pitsavos, C. Chrysochoou, D. Panagiotakos, C. Tentolouris, K. Marinou, N. Koumallos, and C. Stefanadis Genetic Polymorphism on Endothelial Nitric Oxide Synthase Affects Endothelial Activation and Inflammatory Response During the Acute Phase of Myocardial Infarction J. Am. Coll. Cardiol., September 20, 2005; 46(6): 1101 - 1109. [Abstract] [Full Text] [PDF]
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T. Munzel, A. Daiber, V. Ullrich, and A. Mulsch Vascular Consequences of Endothelial Nitric Oxide Synthase Uncoupling for the Activity and Expression of the Soluble Guanylyl Cyclase and the cGMP-Dependent Protein Kinase Arterioscler Thromb Vasc Biol, August 1, 2005; 25(8): 1551 - 1557. [Abstract] [Full Text] [PDF]
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J. E. Barbato, B. S. Zuckerbraun, M. Overhaus, K. G. Raman, and E. Tzeng Nitric oxide modulates vascular inflammation and intimal hyperplasia in insulin resistance and the metabolic syndrome Am J Physiol Heart Circ Physiol, July 1, 2005; 289(1): H228 - H236. [Abstract] [Full Text] [PDF]
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Y. Taniyama, H. Hitomi, A. Shah, R. W. Alexander, and K. K. Griendling Mechanisms of Reactive Oxygen Species-Dependent Downregulation of Insulin Receptor Substrate-1 by Angiotensin II Arterioscler Thromb Vasc Biol, June 1, 2005; 25(6): 1142 - 1147. [Abstract] [Full Text] [PDF]
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M. Satoh, S. Fujimoto, Y. Haruna, S. Arakawa, H. Horike, N. Komai, T. Sasaki, K. Tsujioka, H. Makino, and N. Kashihara NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy Am J Physiol Renal Physiol, June 1, 2005; 288(6): F1144 - F1152. [Abstract] [Full Text] [PDF]
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A. Ergul, J. S. Johansen, C. Stromhaug, A. K. Harris, J. Hutchinson, A. Tawfik, A. Rahimi, E. Rhim, B. Wells, R. W. Caldwell, et al. Vascular Dysfunction of Venous Bypass Conduits Is Mediated by Reactive Oxygen Species in Diabetes: Role of Endothelin-1 J. Pharmacol. Exp. Ther., April 1, 2005; 313(1): 70 - 77. [Abstract] [Full Text] [PDF]
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A. F. Dominiczak, D. Graham, M. W. McBride, N. J.R. Brain, W. K. Lee, F. J. Charchar, M. Tomaszewski, C. Delles, and C. A. Hamilton Cardiovascular Genomics and Oxidative Stress Hypertension, April 1, 2005; 45(4): 636 - 642. [Abstract] [Full Text] [PDF]
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I. S. Thrainsdottir, T. Aspelund, G. Thorgeirsson, V. Gudnason, T. Hardarson, K. Malmberg, G. Sigurdsson, and L. Ryden The Association Between Glucose Abnormalities and Heart Failure in the Population-Based Reykjavik Study Diabetes Care, March 1, 2005; 28(3): 612 - 616. [Abstract] [Full Text] [PDF]
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S. A. Summers and D. H. Nelson A Role for Sphingolipids in Producing the Common Features of Type 2 Diabetes, Metabolic Syndrome X, and Cushing's Syndrome Diabetes, March 1, 2005; 54(3): 591 - 602. [Abstract] [Full Text] [PDF]
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C. Rask-Madsen and G. L. King Proatherosclerotic Mechanisms Involving Protein Kinase C in Diabetes and Insulin Resistance Arterioscler Thromb Vasc Biol, March 1, 2005; 25(3): 487 - 496. [Abstract] [Full Text] [PDF]
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J. Bauersachs and A. Schafer Tetrahydrobiopterin and eNOS dimer/monomer ratio-a clue to eNOS uncoupling in diabetes? Cardiovasc Res, March 1, 2005; 65(4): 768 - 769. [Full Text] [PDF]
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A. Huang, Y.-Y. Zhang, K. Chen, K. Hatakeyama, and J. F. Keaney Jr Cytokine-Stimulated GTP Cyclohydrolase I Expression in Endothelial Cells Requires Coordinated Activation of Nuclear Factor-{kappa}B and Stat1/Stat3 Circ. Res., February 4, 2005; 96(2): 164 - 171. [Abstract] [Full Text] [PDF]
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N. Lu, B. G. Helwig, R. J. Fels, S. Parimi, and M. J. Kenney Central Tempol alters basal sympathetic nerve discharge and attenuates sympathetic excitation to central ANG II Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2626 - H2633. [Abstract] [Full Text] [PDF]
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 J.-M. Li and A. M Shah Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2004; 287(5): R1014 - R1030. [Abstract] [Full Text] [PDF]
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J.-D. Luo, Y.-Y. Wang, W.-L. Fu, J. Wu, and A. F. Chen Gene Therapy of Endothelial Nitric Oxide Synthase and Manganese Superoxide Dismutase Restores Delayed Wound Healing in Type 1 Diabetic Mice Circulation, October 19, 2004; 110(16): 2484 - 2493. [Abstract] [Full Text] [PDF]
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K. Witte, J. Hachenberger, M. F. Castell, C. F. Vahl, and C. Haller Nitric Oxide-Sensitive Soluble Guanylyl Cyclase Activity Is Preserved in Internal Mammary Artery of Type 2 Diabetic Patients Diabetes, October 1, 2004; 53(10): 2640 - 2644. [Abstract] [Full Text] [PDF]
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S. Wassmann, K. Wassmann, and G. Nickenig Modulation of Oxidant and Antioxidant Enzyme Expression and Function in Vascular Cells Hypertension, October 1, 2004; 44(4): 381 - 386. [Abstract] [Full Text] [PDF]
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A. Prasad and A. A. Quyyumi Renin-Angiotensin System and Angiotensin Receptor Blockers in the Metabolic Syndrome Circulation, September 14, 2004; 110(11): 1507 - 1512. [Full Text] [PDF]
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T. J. Guzik, J. Sadowski, B. Kapelak, A. Jopek, P. Rudzinski, R. Pillai, R. Korbut, and K. M. Channon Systemic Regulation of Vascular NAD(P)H Oxidase Activity and Nox Isoform Expression in Human Arteries and Veins Arterioscler Thromb Vasc Biol, September 1, 2004; 24(9): 1614 - 1620. [Abstract] [Full Text] [PDF]
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 G.T. Chew and G.F. Watts Coenzyme Q10 and diabetic endotheliopathy: oxidative stress and the 'recoupling hypothesis' QJM, August 1, 2004; 97(8): 537 - 548. [Abstract] [Full Text] [PDF]
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S. Veerareddy, C.-L. M. Cooke, P. N. Baker, and S. T. Davidge Gender differences in myogenic tone in superoxide dismutase knockout mouse: animal model of oxidative stress Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H40 - H45. [Abstract] [Full Text] [PDF]
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J. Q. Liu and R. J. Folz Extracellular superoxide enhances 5-HT-induced murine pulmonary artery vasoconstriction Am J Physiol Lung Cell Mol Physiol, July 1, 2004; 287(1): L111 - L118. [Abstract] [Full Text] [PDF]
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F Violi, L Loffredo, L Musella, and A Marcoccia Should antioxidant status be considered in interventional trials with antioxidants? Heart, June 1, 2004; 90(6): 598 - 602. [Abstract] [Full Text] [PDF]
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D. Sigaudo-Roussel, C. Demiot, B. Fromy, A. Koitka, G. Leftheriotis, P. Abraham, and J. L. Saumet Early Endothelial Dysfunction Severely Impairs Skin Blood Flow Response to Local Pressure Application in Streptozotocin-Induced Diabetic Mice Diabetes, June 1, 2004; 53(6): 1564 - 1569. [Abstract] [Full Text] [PDF]
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A M Shah and K M Channon Free radicals and redox signalling in cardiovascular disease Heart, May 1, 2004; 90(5): 486 - 487. [Full Text] [PDF]
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B. Erdos, J. A. Snipes, A. W. Miller, and D. W. Busija Cerebrovascular Dysfunction in Zucker Obese Rats Is Mediated by Oxidative Stress and Protein Kinase C Diabetes, May 1, 2004; 53(5): 1352 - 1359. [Abstract] [Full Text] [PDF]
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I. Eskurza, K. D. Monahan, J. A. Robinson, and D. R. Seals Ascorbic acid does not affect large elastic artery compliance or central blood pressure in young and older men Am J Physiol Heart Circ Physiol, April 1, 2004; 286(4): H1528 - H1534. [Abstract] [Full Text] [PDF]
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 B. Erdos, S. A. Simandle, J. A. Snipes, A. W. Miller, and D. W. Busija Potassium Channel Dysfunction in Cerebral Arteries of Insulin-Resistant Rats Is Mediated by Reactive Oxygen Species Stroke, April 1, 2004; 35(4): 964 - 969. [Abstract] [Full Text] [PDF]
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N. J. Alp and K. M. Channon Regulation of Endothelial Nitric Oxide Synthase by Tetrahydrobiopterin in Vascular Disease Arterioscler Thromb Vasc Biol, March 1, 2004; 24(3): 413 - 420. [Abstract] [Full Text]
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