© 1998 American Heart Association, Inc.
Original Contributions |
Reduced Nitric Oxide Production and Altered Myocardial Metabolism During the Decompensation of Pacing-Induced Heart Failure in the Conscious Dog
From the Department of Physiology, New York Medical College, Valhalla.
Correspondence to Thomas Hintze, PhD, Department of Physiology, New York Medical College, Valhalla, NY 10595. E-mail Thomas_Hintze{at}nymc.edu
Abstract—The aim of the present study was to determine whether cardiac nitric oxide (NO) production changes during the progression of pacing-induced heart failure and whether this occurs in association with alterations in myocardial metabolism. Dogs (n=8) were instrumented and the heart paced until left ventricular end-diastolic pressure reached 25 mm Hg and clinical signs of severe failure were evident. Every week, hemodynamic measurements were recorded and blood samples were withdrawn from the aorta and the coronary sinus for measurement of NO metabolites, O2 content, free fatty acids (FFAs), and lactate and glucose concentrations. Cardiac production of NO metabolites or consumption of O2 or utilization of substrates was calculated as coronary sinus-arterial difference times coronary flow. In end-stage failure, occurring at 29±1.6 days, left ventricular end-diastolic pressure was 25±1 mm Hg, left ventricular systolic pressure was 92±3 mm Hg, mean arterial pressure was 75±2.5 mm Hg, and dP/dtmax was 1219±73 mm Hg/s (all P<0.05). These changes in hemodynamics were associated with a fall of cardiac NO metabolite production from 0.37±0.16 to -0.28±0.13 nmol/beat (P<0.05). O2 consumption and lactate uptake did not change significantly from control, while FFA uptake decreased from 0.16±0.03 to 0.05±0.01 µEq/beat and glucose uptake increased from -2.3±7.0 to 41±10 µg/beat (P<0.05). The cardiac respiratory quotient also increased significantly by 28%. In 14 normal dogs the same measurements were performed at control and 1 hour after we injected 30 mg/kg of nitro-L-arginine, a competitive inhibitor of NO synthase. O2 consumption increased from 0.05±0.002 mL/beat at control to 0.071±0.003 mL/beat after nitro-L-arginine, while FFA uptake decreased from 0.1±0.01 to 0.06±0.01 µEq/beat, lactate uptake increased from 0.15±0.04 to 0.31±0.03 µmol/beat, glucose uptake increased from 8.2±5.0 to 35.4±9.5 µg/beat, and RQ increased by 23% (all P<0.05). Our results indicate that basal cardiac production of NO falls below normal levels during cardiac decompensation and that there are shifts in substrate utilization. This switch in myocardial substrate utilization also occurs after acute pharmacological blockade of NO production in normal dogs.
Key Words: MVO2 • lactate • free fatty acid • glucose • respiratory quotient
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J. M. Cotton, M. T. Kearney, P. A. MacCarthy, R. M. Grocott-Mason, D. R. McClean, C. Heymes, P. J. Richardson, and A. M. Shah Effects of Nitric Oxide Synthase Inhibition on Basal Function and the Force-Frequency Relationship in the Normal and Failing Human Heart In Vivo Circulation, November 6, 2001; 104(19): 2318 - 2323. [Abstract] [Full Text] [PDF]
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 S. Adler, H. Huang, J. N. Trochu, X. Xu, S. Gupta, and T. H. Hintze Simvastatin reverses impaired regulation of renal oxygen consumption in congestive heart failure Am J Physiol Renal Physiol, November 1, 2001; 281(5): F802 - F809. [Abstract] [Full Text] [PDF]
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D. J. Grieve, P. A. MacCarthy, N. P. Gall, A. C. Cave, and A. M. Shah Divergent Biological Actions of Coronary Endothelial Nitric Oxide During Progression of Cardiac Hypertrophy Hypertension, August 1, 2001; 38(2): 267 - 273. [Abstract] [Full Text] [PDF]
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Y. Kakinuma, T. Miyauchi, K. Yuki, N. Murakoshi, K. Goto, and I. Yamaguchi Novel Molecular Mechanism of Increased Myocardial Endothelin-1 Expression in the Failing Heart Involving the Transcriptional Factor Hypoxia-Inducible Factor-1{{alpha}} Induced for Impaired Myocardial Energy Metabolism Circulation, May 15, 2001; 103(19): 2387 - 2394. [Abstract] [Full Text] [PDF]
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S. Adler, H. Huang, K. E. Loke, X. Xu, H. Tada, A. Laumas, and T. H. Hintze Endothelial nitric oxide synthase plays an essential role in regulation of renal oxygen consumption by NO Am J Physiol Renal Physiol, May 1, 2001; 280(5): F838 - F843. [Abstract] [Full Text] [PDF]
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K. E Loke, E. J Messina, E. G Shesely, G. Kaley, and T. H Hintze Potential role of eNOS in the therapeutic control of myocardial oxygen consumption by ACE inhibitors and amlodipine Cardiovasc Res, January 1, 2001; 49(1): 86 - 93. [Abstract] [Full Text] [PDF]
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G. S. Nelson, R. D. Berger, B. J. Fetics, M. Talbot, J. C. Spinelli, J. M. Hare, and D. A. Kass Left Ventricular or Biventricular Pacing Improves Cardiac Function at Diminished Energy Cost in Patients With Dilated Cardiomyopathy and Left Bundle-Branch Block Circulation, December 19, 2000; 102(25): 3053 - 3059. [Abstract] [Full Text] [PDF]
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J.-N. Trochu, J.-B. Bouhour, G. Kaley, and T. H. Hintze Role of Endothelium-Derived Nitric Oxide in the Regulation of Cardiac Oxygen Metabolism : Implications in Health and Disease Circ. Res., December 8, 2000; 87(12): 1108 - 1117. [Abstract] [Full Text] [PDF]
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S. Mital, X. Zhang, G. Zhao, R. D. Bernstein, C. J. Smith, D. L. Fulton, W. C. Sessa, J. K. Liao, and T. H. Hintze Simvastatin upregulates coronary vascular endothelial nitric oxide production in conscious dogs Am J Physiol Heart Circ Physiol, December 1, 2000; 279(6): H2649 - H2657. [Abstract] [Full Text] [PDF]
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S. Mital, K. E. Loke, L. J. Addonizio, M. C. Oz, and T. H. Hintze Left ventricular assist device implantation augments nitric oxide dependent control of mitochondrial respiration in failing human hearts J. Am. Coll. Cardiol., November 15, 2000; 36(6): 1897 - 1902. [Abstract] [Full Text] [PDF]
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Y.-T. Shen, P. S Buie, J. J Lynch, S. M Krause, and X.-L. Ma Chronic therapy with an ETA/B receptor antagonist in conscious dogs during progression of congestive heart failure: Intracellular Ca2+ regulation and nitric oxide mediated coronary relaxation Cardiovasc Res, November 1, 2000; 48(2): 332 - 345. [Abstract] [Full Text] [PDF]
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 P. Kinnunen, I. Szokodi, M. G. Nicholls, and H. Ruskoaho Impact of NO on ET-1- and AM-induced inotropic responses: potentiation by combined administration Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2000; 279(2): R569 - R575. [Abstract] [Full Text] [PDF]
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F. A. Recchia, T. R. Vogel, and T. H. Hintze NO metabolites accumulate in erythrocytes in proportion to carbon dioxide and bicarbonate concentration Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H852 - H856. [Abstract] [Full Text] [PDF]
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J. M. Canty Jr. Nitric Oxide and Short-Term Hibernation : Friend or Foe? Circ. Res., July 21, 2000; 87(2): 85 - 87. [Full Text] [PDF]
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S. Kanno, P. C. Lee, Y. Zhang, C. Ho, B. P. Griffith, L. L. Shears II, and T. R. Billiar Attenuation of Myocardial Ischemia/Reperfusion Injury by Superinduction of Inducible Nitric Oxide Synthase Circulation, June 13, 2000; 101(23): 2742 - 2748. [Abstract] [Full Text] [PDF]
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J. M. Hare, R. A. Lofthouse, G. J. Juang, L. Colman, K. M. Ricker, B. Kim, H. Senzaki, S. Cao, R. S. Tunin, and D. A. Kass Contribution of Caveolin Protein Abundance to Augmented Nitric Oxide Signaling in Conscious Dogs With Pacing-Induced Heart Failure Circ. Res., May 26, 2000; 86(10): 1085 - 1092. [Abstract] [Full Text] [PDF]
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S. D. Prabhu, B. Chandrasekar, D. R. Murray, and G. L. Freeman {beta}-Adrenergic Blockade in Developing Heart Failure : Effects on Myocardial Inflammatory Cytokines, Nitric Oxide, and Remodeling Circulation, May 2, 2000; 101(17): 2103 - 2109. [Abstract] [Full Text] [PDF]
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H. Tada, C. I. Thompson, F. A. Recchia, K. E. Loke, M. Ochoa, C. J. Smith, E. G. Shesely, G. Kaley, and T. H. Hintze Myocardial Glucose Uptake Is Regulated by Nitric Oxide via Endothelial Nitric Oxide Synthase in Langendorff Mouse Heart Circ. Res., February 18, 2000; 86(3): 270 - 274. [Abstract] [Full Text] [PDF]
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D. Sun, A. Huang, G. Zhao, R. Bernstein, P. Forfia, X. Xu, A. Koller, G. Kaley, and T. H. Hintze Reduced NO-dependent arteriolar dilation during the development of cardiomyopathy Am J Physiol Heart Circ Physiol, February 1, 2000; 278(2): H461 - H468. [Abstract] [Full Text] [PDF]
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C. Depre and H. Taegtmeyer Metabolic aspects of programmed cell survival and cell death in the heart Cardiovasc Res, February 1, 2000; 45(3): 538 - 548. [Abstract] [Full Text] [PDF]
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P. A. MacCarthy, R. Grocott-Mason, B. D. Prendergast, and A. M. Shah Contrasting Inotropic Effects of Endogenous Endothelin in the Normal and Failing Human Heart : Studies With an Intracoronary ETA Receptor Antagonist Circulation, January 18, 2000; 101(2): 142 - 147. [Abstract] [Full Text] [PDF]
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 F. A. Recchia, R. D. Bernstein, P. B. Sehgal, N. R. Ferreri, and T. H. Hintze Cytokines Are Not a Requisite Part of the Pathophysiology Leading to Cardiac Decompensation Experimental Biology and Medicine, January 1, 2000; 223(1): 47 - 52. [Abstract] [Full Text]
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F. A. Recchia, P. I. McConnell, K. E. Loke, X. Xu, M. Ochoa, and T. H. Hintze Nitric oxide controls cardiac substrate utilization in the conscious dog Cardiovasc Res, November 1, 1999; 44(2): 325 - 332. [Abstract] [Full Text] [PDF]
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K. E. Loke, S. K. Laycock, S. Mital, M. S. Wolin, R. Bernstein, M. Oz, L. Addonizio, G. Kaley, and T. H. Hintze Nitric Oxide Modulates Mitochondrial Respiration in Failing Human Heart Circulation, September 21, 1999; 100(12): 1291 - 1297. [Abstract] [Full Text] [PDF]
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W. J Paulus and A. M Shah NO and cardiac diastolic function Cardiovasc Res, August 15, 1999; 43(3): 595 - 606. [Full Text] [PDF]
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H. Drexler Nitric Oxide Synthases in the Failing Human Heart : A Doubled-Edged Sword? Circulation, June 15, 1999; 99(23): 2972 - 2975. [Full Text] [PDF]
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C. Heymes, M. Vanderheyden, J. G. F. Bronzwaer, A. M. Shah, and W. J. Paulus Endomyocardial Nitric Oxide Synthase and Left Ventricular Preload Reserve in Dilated Cardiomyopathy Circulation, June 15, 1999; 99(23): 3009 - 3016. [Abstract] [Full Text] [PDF]
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J. S. Ingwall and R. A. Kelly Nitric Oxide, Myocardial Oxygen Consumption, and ATP Synthesis Circ. Res., November 16, 1998; 83(10): 1067 - 1068. [Full Text] [PDF]
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D. B. Haitsma, D. Merkus, J. Vermeulen, P. D. Verdouw, and D. J. Duncker Nitric oxide production is maintained in exercising swine with chronic left ventricular dysfunction Am J Physiol Heart Circ Physiol, June 1, 2002; 282(6): H2198 - H2209. [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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