© 1998 American Heart Association, Inc.
Original Contributions |
Superoxide Production in Vascular Smooth Muscle Contributes to Oxidative Stress and Impaired Relaxation in Atherosclerosis
From the Department of Internal Medicine, University of Iowa College of Medicine and Cardiovascular Center, and Veterans Administration Medical Center, Iowa City, Iowa.
Correspondence to Francis J. Miller, Jr, MD, E315 General Hospital, Department of Internal Medicine, University of Iowa Hospitals, Iowa City, IA 52242. E-mail francis-miller{at}uiowa.edu
Abstract—The endothelium is a source of reactive oxygen species in short-term models of hypercholesterolemia and atherosclerosis. We examined a chronic model of atherosclerosis for increased vascular production of superoxide (O2-·) and determined whether endothelial overexpression of superoxide dismutase (SOD) would improve endothelium-dependent relaxation. Superoxide generation was 3 times higher in isolated aortas from Watanabe heritable hyperlipidemic (WHHL) rabbits (2 to 4 years old) compared with aortas from New Zealand White (NZ) rabbits (43±10 versus 14±2 relative light units · min-1 · mm-2, n=9, P<0.05). After in vitro transduction with adenovirus containing the gene for CuZn-SOD (AdCMVCuZn-SOD) or extracellular SOD (AdCMVEC-SOD), endothelial O2-· levels in WHHL aortas were significantly reduced. Gene transfer of SOD to WHHL aortas, however, failed to improve the impaired relaxation to acetylcholine or calcium ionophore. By use of the oxidative fluorescent dye hydroethidine, an in situ assay indicated markedly increased generation of O2-· throughout the wall of WHHL aorta, especially within layers of smooth muscle. This finding was confirmed by demonstrating increased O2-· levels in smooth muscle cells cultured from WHHL aorta. We conclude that elevated O2-· levels in atherosclerotic vessels are not confined to the endothelium but occur throughout the vascular wall, including smooth muscle cells. Reduction in endothelial O2-· levels is not sufficient to improve endothelium-dependent relaxation. Generation of reactive oxygen species within the media may contribute to vasomotor dysfunction in atherosclerosis.
Key Words: superoxide dismutase • reactive oxygen species • gene transfer • adenovirus • acetylcholine • atherosclerosis
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D. D. Gutterman, H. Miura, and Y. Liu Redox Modulation of Vascular Tone: Focus of Potassium Channel Mechanisms of Dilation Arterioscler. Thromb. Vasc. Biol., April 1, 2005; 25(4): 671 - 678. [Abstract] [Full Text] [PDF]
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S. A. Phillips, F. A. Sylvester, and J. C. Frisbee Oxidant stress and constrictor reactivity impair cerebral artery dilation in obese Zucker rats Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2005; 288(2): R522 - R530. [Abstract] [Full Text] [PDF]
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S. P. Didion and F. M. Faraci Ceramide-Induced Impairment of Endothelial Function Is Prevented by CuZn Superoxide Dismutase Overexpression Arterioscler. Thromb. Vasc. Biol., January 1, 2005; 25(1): 90 - 95. [Abstract] [Full Text] [PDF]
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S.-i. Yamagishi, R. Abe, Y. Inagaki, K. Nakamura, H. Sugawara, D. Inokuma, H. Nakamura, T. Shimizu, M. Takeuchi, A. Yoshimura, et al. Minodronate, a Newly Developed Nitrogen-Containing Bisphosphonate, Suppresses Melanoma Growth and Improves Survival in Nude Mice by Blocking Vascular Endothelial Growth Factor Signaling Am. J. Pathol., December 1, 2004; 165(6): 1865 - 1874. [Abstract] [Full Text] [PDF]
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A. D. Nguyen, S. Itoh, V. Jeney, H. Yanagisawa, M. Fujimoto, M. Ushio-Fukai, and T. Fukai Fibulin-5 Is a Novel Binding Protein for Extracellular Superoxide Dismutase Circ. Res., November 26, 2004; 95(11): 1067 - 1074. [Abstract] [Full Text] [PDF]
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K. Sato, T. Komaru, H. Shioiri, S. Takeda, K. Takahashi, H. Kanatsuka, M. Nakayama, and K. Shirato Hypercholesterolemia Impairs Transduction of Vasodilator Signals Derived From Ischemic Myocardium: Myocardium-Microvessel Cross-Talk Arterioscler. Thromb. Vasc. Biol., November 1, 2004; 24(11): 2034 - 2039. [Abstract] [Full Text] [PDF]
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R. Stocker, A. Huang, E. Jeranian, J. Y. Hou, T. T. Wu, S. R. Thomas, and J. F. Keaney Jr Hypochlorous Acid Impairs Endothelium-Derived Nitric Oxide Bioactivity Through a Superoxide-Dependent Mechanism Arterioscler. Thromb. Vasc. Biol., November 1, 2004; 24(11): 2028 - 2033. [Abstract] [Full Text] [PDF]
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J. J. Andresen, F. M. Faraci, and D. D. Heistad Vasomotor responses in MnSOD-deficient mice Am J Physiol Heart Circ Physiol, September 1, 2004; 287(3): H1141 - H1148. [Abstract] [Full Text] [PDF]
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T. Anazawa, P. C. Dimayuga, H. Li, S. Tani, J. Bradfield, K.-Y. Chyu, S. Kaul, P. K. Shah, and B. Cercek Effect of Exposure to Cigarette Smoke on Carotid Artery Intimal Thickening: The Role of Inducible NO Synthase Arterioscler. Thromb. Vasc. Biol., September 1, 2004; 24(9): 1652 - 1658. [Abstract] [Full Text] [PDF]
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Z. Chen, J. F. Keaney Jr., E. Schulz, B. Levison, L. Shan, M. Sakuma, X. Zhang, C. Shi, S. L. Hazen, and D. I. Simon Decreased neointimal formation in Nox2-deficient mice reveals a direct role for NADPH oxidase in the response to arterial injury PNAS, August 31, 2004; 101(35): 13014 - 13019. [Abstract] [Full Text] [PDF]
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D. D. Lund, C. A. Gunnett, Y. Chu, R. M. Brooks, F. M. Faraci, and D. D. Heistad Gene transfer of extracellular superoxide dismutase improves relaxation of aorta after treatment with endotoxin Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H805 - H811. [Abstract] [Full Text] [PDF]
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F. M. Faraci and S. P. Didion Vascular Protection: Superoxide Dismutase Isoforms in the Vessel Wall Arterioscler. Thromb. Vasc. Biol., August 1, 2004; 24(8): 1367 - 1373. [Abstract] [Full Text] [PDF]
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S. Dayal, E. Arning, T. Bottiglieri, R. H. Boger, C. D. Sigmund, F. M. Faraci, and S. R. Lentz Cerebral Vascular Dysfunction Mediated by Superoxide in Hyperhomocysteinemic Mice Stroke, August 1, 2004; 35(8): 1957 - 1962. [Abstract] [Full Text] [PDF]
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R. Hernanz, A. M. Briones, M. J. Alonso, E. Vila, and M. Salaices Hypertension alters role of iNOS, COX-2, and oxidative stress in bradykinin relaxation impairment after LPS in rat cerebral arteries Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H225 - H234. [Abstract] [Full Text] [PDF]
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B. S Conklin, W. Fu, P. H Lin, A. B Lumsden, Q. Yao, and C. Chen HIV protease inhibitor ritonavir decreases endothelium-dependent vasorelaxation and increases superoxide in porcine arteries Cardiovasc Res, July 1, 2004; 63(1): 168 - 175. [Abstract] [Full Text] [PDF]
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T. Tanimoto, A. O. Lungu, and B. C. Berk Sphingosine 1-Phosphate Transactivates the Platelet-Derived Growth Factor {beta} Receptor and Epidermal Growth Factor Receptor in Vascular Smooth Muscle Cells Circ. Res., April 30, 2004; 94(8): 1050 - 1058. [Abstract] [Full Text] [PDF]
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M. M. Tarpey, D. A. Wink, and M. B. Grisham Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2004; 286(3): R431 - R444. [Abstract] [Full Text] [PDF]
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J. Cornelissen, J. Armstrong, and C. M. Holt Mechanical Stretch Induces Phosphorylation of p38-MAPK and Apoptosis in Human Saphenous Vein Arterioscler. Thromb. Vasc. Biol., March 1, 2004; 24(3): 451 - 456. [Abstract] [Full Text]
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D. J. Granville, B. Tashakkor, C. Takeuchi, A. B. Gustafsson, C. Huang, M. R. Sayen, P. Wentworth Jr., M. Yeager, and R. A. Gottlieb Reduction of ischemia and reperfusion-induced myocardial damage by cytochrome P450 inhibitors PNAS, February 3, 2004; 101(5): 1321 - 1326. [Abstract] [Full Text] [PDF]
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J. J. Khatri, C. Johnson, R. Magid, S. M. Lessner, K. M. Laude, S. I. Dikalov, D. G. Harrison, H.-J. Sung, Y. Rong, and Z. S. Galis Vascular Oxidant Stress Enhances Progression and Angiogenesis of Experimental Atheroma Circulation, February 3, 2004; 109(4): 520 - 525. [Abstract] [Full Text] [PDF]
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P. L. Nerheim, J. L. Meier, M. A. Vasef, W.-G. Li, L. Hu, J. B. Rice, D. Gavrila, W. E. Richenbacher, and N. L. Weintraub Enhanced Cytomegalovirus Infection in Atherosclerotic Human Blood Vessels Am. J. Pathol., February 1, 2004; 164(2): 589 - 600. [Abstract] [Full Text] [PDF]
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T. Ago, T. Kitazono, H. Ooboshi, T. Iyama, Y. H. Han, J. Takada, M. Wakisaka, S. Ibayashi, H. Utsumi, and M. Iida Nox4 as the Major Catalytic Component of an Endothelial NAD(P)H Oxidase Circulation, January 20, 2004; 109(2): 227 - 233. [Abstract] [Full Text] [PDF]
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K. K.W. Au-Yeung, C. W.H. Woo, F. L. Sung, J. C.W. Yip, Y. L. Siow, and K. O Hyperhomocysteinemia Activates Nuclear Factor-{kappa}B in Endothelial Cells via Oxidative Stress Circ. Res., January 9, 2004; 94(1): 28 - 36. [Abstract] [Full Text] [PDF]
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T. Bleeke, H. Zhang, N. Madamanchi, C. Patterson, and J. E. Faber Catecholamine-Induced Vascular Wall Growth Is Dependent on Generation of Reactive Oxygen Species Circ. Res., January 9, 2004; 94(1): 37 - 45. [Abstract] [Full Text] [PDF]
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A. H. Chamseddine and F. J. Miller Jr. gp91phox Contributes to NADPH oxidase activity in aortic fibroblasts but not smooth muscle cells Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2284 - H2289. [Abstract] [Full Text] [PDF]
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D. Lebrecht, B. Setzer, U.-P. Ketelsen, J. Haberstroh, and U. A. Walker Time-Dependent and Tissue-Specific Accumulation of mtDNA and Respiratory Chain Defects in Chronic Doxorubicin Cardiomyopathy Circulation, November 11, 2003; 108(19): 2423 - 2429. [Abstract] [Full Text] [PDF]
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W. Gu, D. Weihrauch, K. Tanaka, J. P. Tessmer, P. S. Pagel, J. R. Kersten, W. M. Chilian, and D. C. Warltier Reactive oxygen species are critical mediators of coronary collateral development in a canine model Am J Physiol Heart Circ Physiol, October 1, 2003; 285(4): H1582 - H1589. [Abstract] [Full Text] [PDF]
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J. B. Rice, L. L. Stoll, W.-G. Li, G. M. Denning, J. Weydert, E. Charipar, W. E. Richenbacher, F. J. Miller Jr, and N. L. Weintraub Low-Level Endotoxin Induces Potent Inflammatory Activation of Human Blood Vessels: Inhibition by Statins Arterioscler. Thromb. Vasc. Biol., September 1, 2003; 23(9): 1576 - 1582. [Abstract] [Full Text] [PDF]
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X. Gu, A. B. El-Remessy, S. E. Brooks, M. Al-Shabrawey, N.-T. Tsai, and R. B. Caldwell Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite Am J Physiol Cell Physiol, September 1, 2003; 285(3): C546 - C554. [Abstract] [Full Text] [PDF]
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