© 1999 American Heart Association, Inc.
Cellular Biology |
Mitochondrial Electron Transport Complex I Is a Potential Source of Oxygen Free Radicals in the Failing Myocardium
From the Research Institute of Angiocardiology and Cardiovascular Clinic (T.I., H.T., S.K., K.A., K.E., A.T.) and Department of Clinical Chemistry and Laboratory Medicine (H.U.), Kyushu University School of Medicine, Fukuoka, Japan; Department of Biophysics (D.K.), Kyushu University, Fukuoka, Japan; Department of Neurology (N.H.), Juntendo University School of Medicine, Tokyo, Japan; and Laboratory of Food and Biodynamics (K.U.), Nagoya University School of Bioagricultural Sciences, Nagoya, Japan.
Correspondence to Hiroyuki Tsutsui, MD, PhD, Research Institute of Angiocardiology and Cardiovascular Clinic, Kyushu University School of Medicine, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan. E-mail prehiro{at}cardiol.med.kyushu-u.ac.jp
Abstract—Oxidative stress in the myocardium may play an important role in the pathogenesis of congestive heart failure (HF). However, the cellular sources and mechanisms for the enhanced generation of reactive oxygen species (ROS) in the failing myocardium remain unknown. The amount of thiobarbituric acid reactive substances increased in the canine HF hearts subjected to rapid ventricular pacing for 4 weeks, and immunohistochemical staining of 4-hydroxy-2-nonenal ROS-induced lipid peroxides was detected in cardiac myocytes but not in interstitial cells of HF animals. The generation of superoxide anion was directly assessed in the submitochondrial fractions by use of electron spin resonance spectroscopy with spin trapping agent, 5,5'-dimethyl-1-pyrroline-N-oxide, in the presence of NADH and succinate as a substrate for NADH–ubiquinone oxidoreductase (complex I) and succinate–ubiquinone oxidoreductase (complex II), respectively. Superoxide production was increased 2.8-fold (P<0.01) in HF, which was due to the functional block of electron transport at complex I. The enzymatic activity of complex I decreased in HF (274±13 versus 136±9 nmol · min-1 · mg-1 protein, P<0.01), which may thus have caused the functional uncoupling of the respiratory chain and the deleterious ROS production in HF mitochondria. The present study provided direct evidence for the involvement of ROS in the mitochondrial origin of HF myocytes, which might be responsible for both contractile dysfunction and structural damage to the myocardium.
Key Words: antioxidant • free radical • heart failure • myocardial contraction • reactive oxygen species
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S. Srivastava, B. Chandrasekar, A. Bhatnagar, and S. D. Prabhu Lipid peroxidation-derived aldehydes and oxidative stress in the failing heart: role of aldose reductase Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2612 - H2619. [Abstract] [Full Text] [PDF]
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Y. Sun, J. Zhang, L. Lu, S. S. Chen, M. T. Quinn, and K. T. Weber Aldosterone-Induced Inflammation in the Rat Heart : Role of Oxidative Stress Am. J. Pathol., November 1, 2002; 161(5): 1773 - 1781. [Abstract] [Full Text] [PDF]
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P. J Hanley, J. Ray, U. Brandt, and J. Daut Halothane, isoflurane and sevoflurane inhibit NADH: ubiquinone oxidoreductase (complex I) of cardiac mitochondria J. Physiol., November 1, 2002; 544(3): 687 - 693. [Abstract] [Full Text] [PDF]
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P.a. Pacher, L. Liaudet, J. G. Mabley, K. Komjati, and C. Szabo Pharmacologic inhibition of poly(adenosine diphosphate-ribose) polymerase may represent a novel therapeutic approach in chronic heart failure J. Am. Coll. Cardiol., September 4, 2002; 40(5): 1006 - 1016. [Abstract] [Full Text] [PDF]
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P. J Hanley, M. Mickel, M. Loffler, U. Brandt, and J. Daut KATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart J. Physiol., August 1, 2002; 542(3): 735 - 741. [Abstract] [Full Text] [PDF]
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E. Novalija, S. G. Varadarajan, A. K. S. Camara, J. An, Q. Chen, M. L. Riess, N. Hogg, and D. F. Stowe Anesthetic preconditioning: triggering role of reactive oxygen and nitrogen species in isolated hearts Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H44 - H52. [Abstract] [Full Text] [PDF]
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K. Nakamura, K. Kusano, Y. Nakamura, M. Kakishita, K. Ohta, S. Nagase, M. Yamamoto, K. Miyaji, H. Saito, H. Morita, et al. Carvedilol Decreases Elevated Oxidative Stress in Human Failing Myocardium Circulation, June 18, 2002; 105(24): 2867 - 2871. [Abstract] [Full Text] [PDF]
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W. F. Saavedra, N. Paolocci, M. E. St. John, M. W. Skaf, G. C. Stewart, J.-S. Xie, R. W. Harrison, J. Zeichner, D. Mudrick, E. Marban, et al. Imbalance Between Xanthine Oxidase and Nitric Oxide Synthase Signaling Pathways Underlies Mechanoenergetic Uncoupling in the Failing Heart Circ. Res., February 22, 2002; 90(3): 297 - 304. [Abstract] [Full Text] [PDF]
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J. Shite, F. Qin, W. Mao, H. Kawai, S. Y. Stevens, and C.-s. Liang Antioxidant vitamins attenuate oxidative stress and cardiac dysfunction in tachycardia-induced cardiomyopathy J. Am. Coll. Cardiol., November 15, 2001; 38(6): 1734 - 1740. [Abstract] [Full Text] [PDF]
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J. Shiraishi, T. Tatsumi, N. Keira, K. Akashi, A. Mano, S. Yamanaka, S. Matoba, J. Asayama, T. Yaoi, S. Fushiki, et al. Important role of energy-dependent mitochondrial pathways in cultured rat cardiac myocyte apoptosis Am J Physiol Heart Circ Physiol, October 1, 2001; 281(4): H1637 - H1647. [Abstract] [Full Text] [PDF]
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J. M. Hare Oxidative Stress and Apoptosis in Heart Failure Progression Circ. Res., August 3, 2001; 89(3): 198 - 200. [Full Text] [PDF]
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H. Tsutsui, T. Ide, S. Hayashidani, N. Suematsu, T. Shiomi, J. Wen, K.-i. Nakamura, K. Ichikawa, H. Utsumi, and A. Takeshita Enhanced Generation of Reactive Oxygen Species in the Limb Skeletal Muscles From a Murine Infarct Model of Heart Failure Circulation, July 10, 2001; 104(2): 134 - 136. [Abstract] [Full Text] [PDF]
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 T. Suzuki and T. Miyauchi A novel pharmacological action of ET-1 to prevent the cytotoxicity of doxorubicin in cardiomyocytes Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2001; 280(5): R1399 - R1406. [Abstract] [Full Text] [PDF]
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T. Ide, H. Tsutsui, S. Hayashidani, D. Kang, N. Suematsu, K.-i. Nakamura, H. Utsumi, N. Hamasaki, and A. Takeshita Mitochondrial DNA Damage and Dysfunction Associated With Oxidative Stress in Failing Hearts After Myocardial Infarction Circ. Res., March 16, 2001; 88(5): 529 - 535. [Abstract] [Full Text] [PDF]
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 P Klivenyi, E Karg, C Rozsa, R Horvath, S Komoly, I Nemeth, S Turi, and L Vecsei {alpha}-Tocopherol/lipid ratio in blood is decreased in patients with Leber's hereditary optic neuropathy and asymptomatic carriers of the 11778 mtDNA mutation J. Neurol. Neurosurg. Psychiatry, March 1, 2001; 70(3): 359 - 362. [Abstract] [Full Text] [PDF]
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T. Ukai, C.-P. Cheng, H. Tachibana, A. Igawa, Z.-S. Zhang, H.-J. Cheng, and W. C. Little Allopurinol Enhances the Contractile Response to Dobutamine and Exercise in Dogs With Pacing-Induced Heart Failure Circulation, February 6, 2001; 103(5): 750 - 755. [Abstract] [Full Text] [PDF]
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H. Tsutsui, T. Ide, S. Hayashidani, N. Suematsu, H. Utsumi, R. Nakamura, K. Egashira, and A. Takeshita Greater susceptibility of failing cardiac myocytes to oxygen free radical-mediated injury Cardiovasc Res, January 1, 2001; 49(1): 103 - 109. [Abstract] [Full Text] [PDF]
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G. S. Filippatos, B. D. Uhal, H. Tsutsui, T. Ide, S. Kinugawa, A. Takeshita, and H. Utsumi Effects of Amiodarone on Heart Cells Response Circulation, November 14, 2000; 102 (20): e170 - e170. [Full Text] [PDF]
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S. Kinugawa, H. Tsutsui, S. Hayashidani, T. Ide, N. Suematsu, S. Satoh, H. Utsumi, and A. Takeshita Treatment With Dimethylthiourea Prevents Left Ventricular Remodeling and Failure After Experimental Myocardial Infarction in Mice : Role of Oxidative Stress Circ. Res., September 1, 2000; 87(5): 392 - 398. [Abstract] [Full Text] [PDF]
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D. B. Sawyer and W. S. Colucci Mitochondrial Oxidative Stress in Heart Failure : "Oxygen Wastage" Revisited Circ. Res., February 4, 2000; 86(2): 119 - 120. [Full Text] [PDF]
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T. Ide, H. Tsutsui, S. Kinugawa, N. Suematsu, S. Hayashidani, K. Ichikawa, H. Utsumi, Y. Machida, K. Egashira, and A. Takeshita Direct Evidence for Increased Hydroxyl Radicals Originating From Superoxide in the Failing Myocardium Circ. Res., February 4, 2000; 86(2): 152 - 157. [Abstract] [Full Text] [PDF]
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W. F. Saavedra, N. Paolocci, M. E. St. John, M. W. Skaf, G. C. Stewart, J.-S. Xie, R. W. Harrison, J. Zeichner, D. Mudrick, E. Marban, et al. Imbalance Between Xanthine Oxidase and Nitric Oxide Synthase Signaling Pathways Underlies Mechanoenergetic Uncoupling in the Failing Heart Circ. Res., February 22, 2002; 90(3): 297 - 304. [Abstract] [Full Text] [PDF]
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G. D. Thomas, W. Zhang, and R. G. Victor Impaired Modulation of Sympathetic Vasoconstriction in Contracting Skeletal Muscle of Rats With Chronic Myocardial Infarctions : Role of Oxidative Stress Circ. Res., April 27, 2001; 88(8): 816 - 823. [Abstract] [Full Text] [PDF]
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D. R. Pimentel, J. K. Amin, L. Xiao, T. Miller, J. Viereck, J. Oliver-Krasinski, R. Baliga, J. Wang, D. A. Siwik, K. Singh, et al. Reactive Oxygen Species Mediate Amplitude-Dependent Hypertrophic and Apoptotic Responses to Mechanical Stretch in Cardiac Myocytes Circ. Res., August 31, 2001; 89(5): 453 - 460. [Abstract] [Full Text] [PDF]
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