(Circulation. 1999;100:292-298.)
© 1999 American Heart Association, Inc.
Basic Science Reports |
Endothelial Dysfunction in Chronic Myocardial Infarction Despite Increased Vascular Endothelial Nitric Oxide Synthase and Soluble Guanylate Cyclase Expression
Role of Enhanced Vascular Superoxide Production
From the II. Medizinische Klinik, Universitätsklinikum Mannheim, Fakultät für Klinische Medizin Mannheim der Universität Heidelberg, and Institut für Kardiovaskuläre Physiologie, Klinikum der J.W. Goethe-Universität, Frankfurt am Main (A.B., R.B.), Germany.
Correspondence to Dr Johann Bauersachs, II. Medizinische Klinik, Klinikum, Theodor-Kutzer-Ufer, D-68135 Mannheim, Germany. E-mail johann.bauersachs{at}med2.ma.uni-heidelberg.de
Background—Endothelial dysfunction of the peripheral vasculature is a well-known phenomenon in congestive heart failure that contributes to the elevated peripheral resistance; however, the underlying mechanisms have not yet been clarified.
Methods and Results—Dilator responses, the expression of protein and mRNA of the endothelial nitric oxide synthase (eNOS), inducible NOS (iNOS), and soluble guanylate cyclase (sGC), and superoxide anion (O2-) and peroxynitrite production were determined in aortic rings from Wistar rats 8 weeks after myocardial infarction and compared with those in sham-operated animals. In rats with heart failure, the concentration-response curve of the endothelium-dependent vasodilator acetylcholine (after preconstriction with phenylephrine) was significantly shifted to the right, and the maximum relaxation was attenuated. Determination of expression levels of the 2 key enzymes for NO-mediated dilations, eNOS and sGC, revealed a marked upregulation of both enzymes in aortas from rats with heart failure, whereas iNOS expression was not changed. Pretreatment with exogenous superoxide dismutase partially restored the acetylcholine-induced relaxation in aortas from rats with heart failure. Aortic basal and NADH-stimulated O2- production assessed by use of lucigenin-enhanced chemiluminescence was significantly elevated in rats with chronic myocardial infarction. Peroxynitrite-mediated nitration of protein tyrosine residues was not different between the 2 groups of rats.
Conclusions—These results demonstrate that endothelial dysfunction in ischemic heart failure occurs despite an enhanced vascular eNOS and sGC expression and can be attributed to an increase in vascular O2- production by an NADH-dependent oxidase. By inactivation of NO, O2- production appears to be an essential mechanism for the endothelial dysfunction observed in heart failure.
Key Words: endothelium • endothelium-derived factors • myocardial infarction • heart failure • free radicals
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J. A. Wagner, K. Hu, J. Bauersachs, J. Karcher, M. Wiesler, S. K. Goparaju, G. Kunos, and G. Ertl Endogenous cannabinoids mediate hypotension after experimental myocardial infarction J. Am. Coll. Cardiol., December 1, 2001; 38(7): 2048 - 2054. [Abstract] [Full Text] [PDF]
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M. de Lorgeril, P. Salen, M. Accominotti, M. Cadau, J.-P. Steghens, F. Boucher, and J. de Leiris Dietary and blood antioxidants in patients with chronic heart failure. Insights into the potential importance of selenium in heart failure Eur J Heart Fail, December 1, 2001; 3(6): 661 - 669. [Abstract] [Full Text] [PDF]
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 M. Marques, I. Millas, A. Jimenez, E. Garcia-Colis, J. A. Rodriguez-Feo, S. Velasco, A. Barrientos, S. Casado, and A. Lopez-Farre Alteration of the Soluble Guanylate Cyclase System in the Vascular Wall of Lead-Induced Hypertension in Rats J. Am. Soc. Nephrol., December 1, 2001; 12(12): 2594 - 2600. [Abstract] [Full Text] [PDF]
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R. Nakamura, K. Egashira, K. Arimura, Y. Machida, T. Ide, H. Tsutsui, H. Shimokawa, and A. Takeshita Increased inactivation of nitric oxide is involved in impaired coronary flow reserve in heart failure Am J Physiol Heart Circ Physiol, December 1, 2001; 281(6): H2619 - H2625. [Abstract] [Full Text] [PDF]
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G. Wiemer, G. Itter, T. Malinski, and W. Linz Decreased Nitric Oxide Availability in Normotensive and Hypertensive Rats With Failing Hearts After Myocardial Infarction Hypertension, December 1, 2001; 38(6): 1367 - 1371. [Abstract] [Full Text] [PDF]
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G. F. Mitchell, J.-C. Tardif, J. M. O. Arnold, G. Marchiori, T. X. O'Brien, M. E. Dunlap, and M. A. Pfeffer Pulsatile Hemodynamics in Congestive Heart Failure Hypertension, December 1, 2001; 38(6): 1433 - 1439. [Abstract] [Full Text] [PDF]
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S. M. Wildhirt, M. Weis, C. Schulze, N. Conrad, S. Pehlivanli, G. Rieder, G. Enders, W. von Scheidt, and B. Reichart Expression of Endomyocardial Nitric Oxide Synthase and Coronary Endothelial Function in Human Cardiac Allografts Circulation, September 18, 2001; 104 (2009): I-336 - I-343. [Abstract] [Full Text] [PDF]
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J. Bauersachs, I. Fleming, D. Fraccarollo, R. Busse, and G. Ertl Prevention of endothelial dysfunction in heart failure by vitamin E: Attenuation of vascular superoxide anion formation and increase in soluble guanylyl cyclase expression Cardiovasc Res, August 1, 2001; 51(2): 344 - 350. [Abstract] [Full Text] [PDF]
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P. V. Ennezat, S. L. Malendowicz, M. Testa, P. C. Colombo, A. Cohen-Solal, T. Evans, and T. H. LeJemtel Physical training in patients with chronic heart failure enhances the expression of genes encoding antioxidative enzymes J. Am. Coll. Cardiol., July 1, 2001; 38(1): 194 - 198. [Abstract] [Full Text] [PDF]
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 S. M. Wildhirt, M. Weis, C. Schulze, N. Conrad, S. Pehlivanli, G. Rieder, G. Enders, W. von Scheidt, and B. Reichart Coronary flow reserve and nitric oxide synthases after cardiac transplantation in humans Eur. J. Cardiothorac. Surg., June 1, 2001; 19(6): 840 - 847. [Abstract] [Full Text] [PDF]
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A. Mulsch, M. Oelze, S. Kloss, H. Mollnau, A. Topfer, A. Smolenski, U. Walter, J.-P. Stasch, A. Warnholtz, U. Hink, et al. Effects of In Vivo Nitroglycerin Treatment on Activity and Expression of the Guanylyl Cyclase and cGMP-Dependent Protein Kinase and Their Downstream Target Vasodilator-Stimulated Phosphoprotein in Aorta Circulation, May 1, 2001; 103(17): 2188 - 2194. [Abstract] [Full Text] [PDF]
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L. J Wagenaar, H. Buikema, Y. M Pinto, and W. H van Gilst Improvement of endothelial dysfunction in experimental heart failure by chronic RAAS-blockade: ACE-inhibition or AT1-receptor blockade? Journal of Renin-Angiotensin-Aldosterone System, March 1, 2001; 2(1_suppl): S64 - S69. [Abstract] [PDF]
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A.C. Mendes Ribeiro, T.M.C. Brunini, J.C. Ellory, and G.E. Mann Abnormalities in L-arginine transport and nitric oxide biosynthesis in chronic renal and heart failure Cardiovasc Res, March 1, 2001; 49(4): 697 - 712. [Abstract] [Full Text] [PDF]
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H. Cai and D. G. Harrison Endothelial Dysfunction in Cardiovascular Diseases: The Role of Oxidant Stress Circ. Res., November 10, 2000; 87(10): 840 - 844. [Abstract] [Full Text] [PDF]
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K. M. Channon, H. Qian, and S. E. George Nitric Oxide Synthase in Atherosclerosis and Vascular Injury : Insights From Experimental Gene Therapy Arterioscler Thromb Vasc Biol, August 1, 2000; 20(8): 1873 - 1881. [Abstract] [Full Text] [PDF]
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J. Bauersachs, D. Fraccarollo, P. Galuppo, J. Widder, and G. Ertl Endothelin-receptor blockade improves endothelial vasomotor dysfunction in heart failure Cardiovasc Res, July 1, 2000; 47(1): 142 - 149. [Abstract] [Full Text] [PDF]
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A. B. Driss, C. Devaux, D. Henrion, M. Duriez, C. Thuillez, B. I. Levy, and J.-B. Michel Hemodynamic Stresses Induce Endothelial Dysfunction and Remodeling of Pulmonary Artery in Experimental Compensated Heart Failure Circulation, June 13, 2000; 101(23): 2764 - 2770. [Abstract] [Full Text] [PDF]
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T. J. Guzik, N. E. J. West, E. Black, D. McDonald, C. Ratnatunga, R. Pillai, and K. M. Channon Vascular Superoxide Production by NAD(P)H Oxidase : Association With Endothelial Dysfunction and Clinical Risk Factors Circ. Res., May 12, 2000; 86 (9): e85 - e90. [Abstract] [Full Text] [PDF]
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R. P. Brandes, D.-y. Kim, F.-H. Schmitz-Winnenthal, M. Amidi, A. Godecke, A. Mulsch, and R. Busse Increased Nitrovasodilator Sensitivity in Endothelial Nitric Oxide Synthase Knockout Mice : Role of Soluble Guanylyl Cyclase Hypertension, January 1, 2000; 35(1): 231 - 236. [Abstract] [Full Text] [PDF]
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T. Munzel and D. G. Harrison Increased Superoxide in Heart Failure : A Biochemical Baroreflex Gone Awry Circulation, July 20, 1999; 100(3): 216 - 218. [Full Text] [PDF]
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H.-Y. Sohn, M. Keller, T. Gloe, H. Morawietz, U. Rueckschloss, and U. Pohl The Small G-protein Rac Mediates Depolarization-induced Superoxide Formation in Human Endothelial Cells J. Biol. Chem., June 16, 2000; 275(25): 18745 - 18750. [Abstract] [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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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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