© 1996 American Heart Association, Inc.
Articles |
Role of Endothelium-Derived Nitric Oxide in the Modulation of Canine Myocardial Mitochondrial Respiration In Vitro
Implications for the Development of Heart Failure
the Department of Physiology, New York Medical College, Valhalla.
Correspondence to Thomas H. Hintze, PhD, Professor of Physiology, New York Medical College, Valhalla, NY 10595.
The mechanism responsible for the regulation of cardiac function by endogenous nitric oxide (NO) remains unclear. In this investigation, O2 consumption by freshly isolated myocardial muscle segments from the left ventricular free wall of canine hearts was quantified by a Clark-type O2 electrode at 37°C. S-nitroso-N-acetylpenicillamine (SNAP, 9±3% to 50±8%), bradykinin (BK, 14±3% to 30±5%), or carbachol (CCh, 15±4% to 29±4%) significantly attenuated tissue O2 consumption at doses of 10-7 to 10-4 mol/L (mean±SE, P<.05). The effects of BK and CCh, but not SNAP, were blocked by 10-4 mol/L NG-nitro-L-arginine, consistent with both BK and CCh stimulating NO biosynthesis and with SNAP decomposing to release NO, respectively. Similar doses of 8-Br-cGMP caused a respiratory inhibition, but to a lesser extent (9±2% to 14±6%). A mitochondrial uncoupler, 2,4-dinitrophenol (at 1 mmol/L), blocked the effects of 8-Br-cGMP, but not those of SNAP, BK, or CCh, suggesting that the major site of action of NO is on mitochondrial electron transport. Myocardial muscle from dogs with pacing-induced heart failure had a basal O2 consumption rate of 251±21 nmol·min-1·g-1, which was 54% higher than the rate seen in muscle from normal healthy canine hearts. The inhibitory effects of BK and CCh on O2 consumption were not observed in failing cardiac tissue, but SNAP showed an unaltered inhibitory effect. Therefore, our results indicate that NO released from microvascular endothelium by BK, stimulation of muscarinic receptors, and perhaps flow velocity may play an important physiological role in the control of cardiac mitochondrial respiration, and the loss of this regulatory function may contribute to the development of heart failure.
Key Words: bradykinin • cGMP • oxygen consumption • microvascular endothelium • cardiac dysfunction
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F. A. Recchia, P. I. McConnell, R. D. Bernstein, T. R. Vogel, X. Xu, and T. H. Hintze Reduced Nitric Oxide Production and Altered Myocardial Metabolism During the Decompensation of Pacing-Induced Heart Failure in the Conscious Dog Circ. Res., November 16, 1998; 83(10): 969 - 979. [Abstract] [Full Text] [PDF]
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W. Wang Cardiac sympathetic afferent stimulation by bradykinin in heart failure: role of NO and prostaglandins Am J Physiol Heart Circ Physiol, September 1, 1998; 275(3): H783 - H788. [Abstract] [Full Text] [PDF]
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H. Takano, S. Manchikalapudi, X.-L. Tang, Y. Qiu, A. Rizvi, A. K. Jadoon, Q. Zhang, and R. Bolli Nitric Oxide Synthase Is the Mediator of Late Preconditioning Against Myocardial Infarction in Conscious Rabbits Circulation, August 4, 1998; 98(5): 441 - 449. [Abstract] [Full Text] [PDF]
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N. Suto, A. Mikuniya, T. Okubo, H. Hanada, N. Shinozaki, and K. Okumura Nitric oxide modulates cardiac contractility and oxygen consumption without changing contractile efficiency Am J Physiol Heart Circ Physiol, July 1, 1998; 275(1): H41 - H49. [Abstract] [Full Text] [PDF]
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S. K. Laycock, T. Vogel, P. R. Forfia, J. Tuzman, X. Xu, M. Ochoa, C. I. Thompson, A. Nasjletti, and T. H. Hintze Role of Nitric Oxide in the Control of Renal Oxygen Consumption and the Regulation of Chemical Work in the Kidney Circ. Res., June 29, 1998; 82(12): 1263 - 1271. [Abstract] [Full Text] [PDF]
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Y.-W. Xie, P. M. Kaminski, and M. S. Wolin Inhibition of Rat Cardiac Muscle Contraction and Mitochondrial Respiration by Endogenous Peroxynitrite Formation During Posthypoxic Reoxygenation Circ. Res., May 4, 1998; 82(8): 891 - 897. [Abstract] [Full Text] [PDF]
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R. E Klabunde, J. Tse, and H. R Weiss Guanylyl cyclase inhibition reduces contractility and decreases cGMP and cAMP in isolated rat hearts Cardiovasc Res, March 1, 1998; 37(3): 676 - 683. [Abstract] [Full Text] [PDF]
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R. Bolli, S. Manchikalapudi, X.-L. Tang, H. Takano, Y. Qiu, Y. Guo, Q. Zhang, and A. K. Jadoon The Protective Effect of Late Preconditioning Against Myocardial Stunning in Conscious Rabbits Is Mediated by Nitric Oxide Synthase : Evidence That Nitric Oxide Acts Both as a Trigger and as a Mediator of the Late Phase of Ischemic Preconditioning Circ. Res., December 19, 1997; 81(6): 1094 - 1107. [Abstract] [Full Text]
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 J.-L. Balligand and P. J. Cannon Nitric Oxide Synthases and Cardiac Muscle : Autocrine and Paracrine Influences Arterioscler. Thromb. Vasc. Biol., October 1, 1997; 17(10): 1846 - 1858. [Abstract] [Full Text]
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U. Flogel, M. W. Merx, A. Godecke, U. K. M. Decking, and J. Schrader Myoglobin: A scavenger of bioactive NO PNAS, January 16, 2001; 98(2): 735 - 740. [Abstract] [Full Text] [PDF]
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S. Setty, J. D. Tune, and H. F. Downey Nitric oxide modulates right ventricular flow and oxygen consumption during norepinephrine infusion Am J Physiol Heart Circ Physiol, February 1, 2002; 282(2): H696 - H703. [Abstract] [Full Text] [PDF]
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