Circulation. 2003;107:1418-1423
Published online before print March 3, 2003, doi: 10.1161/01.CIR.0000055318.09997.1F
Published online before print March 3, 2003, doi: 10.1161/01.CIR.0000055318.09997.1F
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(Circulation. 2003;107:1418.)
© 2003 American Heart Association, Inc.
Basic Science Reports |
Oxidative Stress Mediates Tumor Necrosis Factor-
–Induced Mitochondrial DNA Damage and Dysfunction in Cardiac Myocytes
From the Departments of Cardiovascular Medicine (N.S., H.T., J.W., M.I., T.I., S.H., T.S., T.K., A.T.) and Clinical Chemistry and Laboratory Medicine (D.K., N.H.), Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
Correspondence to Hiroyuki Tsutsui, MD, PhD, Cardiovascular Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan. E-mail prehiro{at}cardiol.med.kyushu-u.ac.jp
Background— Tumor necrosis factor-
(TNF-) and angiotensin II (Ang II) are implicated in the development and further progression of heart failure, which might be, at least in part, mediated by the production of reactive oxygen species (ROS). However, the cause and consequences of this agonist-mediated ROS production in cardiac myocytes have not been well defined. Recently, we demonstrated that increased ROS production was associated with mitochondrial DNA (mtDNA) damage and dysfunction in failing hearts. We thus investigated whether the direct exposure of cardiac myocytes to TNF- and Ang II in vitro could induce mtDNA damage via production of ROS.
Methods and Results— TNF- increased ROS production within cultured neonatal rat ventricular myocytes after 1 hour, as assessed by 2',7'-dichlorofluorescin diacetate fluorescence microscopy. TNF- also decreased mtDNA copy number by Southern blot analysis in association with complex III activity, which was prevented in the presence of the antioxidant -tocopherol. A direct exposure of myocytes to H2O2 caused a similar decrease in mtDNA copy number. In contrast, Ang II did not affect mtDNA copy number, despite the similar increase in ROS production. TNF-–mediated ROS production and a decrease in mtDNA copy number were inhibited by the sphingomyelinase inhibitor D609. Furthermore, N-acetylsphingosine (C2-ceramide), a synthetic cell-permeable ceramide analogue, increased myocyte ROS production, suggesting that TNF-–mediated ROS production and subsequent mtDNA damage were mediated by the sphingomyelin-ceramide signaling pathway.
Conclusions— The intimate link between TNF-, ROS, and mtDNA damage might play an important role in myocardial remodeling and failure.
Key Words: myocytes • free radicals • heart failure • antioxidants • genes
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