Giorgio Olivetti, M.D., Rakesh Abbi, M.D., Federico Quaini, M.D., Jan Kajstura, Ph.D., Wei Cheng, M.D., James A. Nitahara, M.D., Eugenio Quaini, M.D., Carla Di Loreto, M.D., Carlo A. Beltrami, M.D., Stanislaw Krajewski, M.D., Ph.D., John C. Reed, M.D., Ph.D., and Piero Anversa, M.D.
Background Loss of myocytes is an important mechanism in thedevelopment of cardiac failure of either ischemic or nonischemicorigin. However, whether programmed cell death (apoptosis) isimplicated in the terminal stages of heart failure is not known.We therefore studied the magnitude of myocyte apoptosis in patientswith intractable congestive heart failure.
Methods Myocardial samples were obtained from the hearts of36 patients who underwent cardiac transplantation and from thehearts of 3 patients who died soon after myocardial infarction.Samples from 11 normal hearts were used as controls. Apoptosiswas evaluated histochemically, biochemically, and by a combinationof histochemical analysis and confocal microscopy. The expressionof two proto-oncogenes that influence apoptosis, BCL2 and BAX,was also determined.
Results Heart failure was characterized morphologically by a232-fold increase in myocyte apoptosis and biochemically byDNA laddering (an indicator of apoptosis). The histochemicaldemonstration of DNA-strand breaks in myocyte nuclei was coupledwith the documentation of chromatin condensation and fragmentationby confocal microscopy. All these findings reflect apoptosisof myocytes. The percentage of myocytes labeled with BCL2 (whichprotects cells against apoptosis) was 1.8 times as high in thehearts of patients with cardiac failure as in the normal hearts,whereas labeling with BAX (which promotes apoptosis) remainedconstant. The near doubling of the expression of BCL2 in thecardiac tissue of patients with heart failure was confirmedby Western blotting.
Conclusions Programmed death of myocytes occurs in the decompensatedhuman heart in spite of the enhanced expression of BCL2; thisphenomenon may contribute to the progression of cardiac dysfunction.
Source Information
From the Departments of Medicine (G.O., J.K., W.C., J.A.N., P.A.) and Pathology (R.A.), New York Medical College, Valhalla; the Department of Pathology, University of Parma, Parma, Italy (F.Q.); the Department of Pathology, University of Udine, Udine, Italy (C.D., C.A.B.); the De Gasperis Division of Cardiac Surgery, Milan, Italy (E.Q.); and the Burnham Institute, La Jolla, Calif. (S.K., J.C.R.).
Address reprint requests to Dr. Anversa at the Department of Medicine, Vosburgh Pavilion 302, New York Medical College, Valhalla, NY 10595.
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Khoynezhad, A., Jalali, Z., Tortolani, A. J.
(2004). Apoptosis: Pathophysiology and therapeutic implications for the cardiac surgeon. Ann. Thorac. Surg.
78: 1109-1118
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Engel, D., Peshock, R., Armstong, R. C., Sivasubramanian, N., Mann, D. L.
(2004). Cardiac myocyte apoptosis provokes adverse cardiac remodeling in transgenic mice with targeted TNF overexpression. Am. J. Physiol. Heart Circ. Physiol.
287: H1303-H1311
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Kawai, K., Qin, F., Shite, J., Mao, W., Fukuoka, S., Liang, C.-s.
(2004). Importance of antioxidant and antiapoptotic effects of {beta}-receptor blockers in heart failure therapy. Am. J. Physiol. Heart Circ. Physiol.
287: H1003-H1012
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Ahmet, I., Krawczyk, M., Heller, P., Moon, C., Lakatta, E. G., Talan, M. I.
(2004). Beneficial Effects of Chronic Pharmacological Manipulation of {beta}-Adrenoreceptor Subtype Signaling in Rodent Dilated Ischemic Cardiomyopathy. Circulation
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Depre, C., Kim, S.-J., John, A. S., Huang, Y., Rimoldi, O. E., Pepper, J. R., Dreyfus, G. D., Gaussin, V., Pennell, D. J., Vatner, D. E., Camici, P. G., Vatner, S. F.
(2004). Program of Cell Survival Underlying Human and Experimental Hibernating Myocardium. Circ. Res.
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Landesberg, G., Mosseri, M., Shatz, V., Akopnik, I., Bocher, M., Mayer, M., Anner, H., Berlatzky, Y., Weissman, C.
(2004). Cardiac troponin after major vascular surgery: The role of perioperative ischemia, preoperative thallium scanning, and coronary revascularization. J Am Coll Cardiol
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Yeh, C.-H., Lin, Y.-M., Wu, Y.-C., Wang, Y.-C., Lin, P. J.
(2004). Nitric oxide attenuates cardiomyocytic apoptosis via diminished mitochondrial complex I up-regulation from cardiac ischemia-reperfusion injury under cardiopulmonary bypass. J. Thorac. Cardiovasc. Surg.
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Yamashita, H., Akamine, S., Sumida, Y., Inoue, M., Sawada, T., Nagayasu, T., Oka, T.
(2004). Inhaled nitric oxide attenuates apoptosis in ischemia-reperfusion injury of the rabbit lung. Ann. Thorac. Surg.
78: 292-297
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Fischer, U. M., Tossios, P., Huebner, A., Geissler, H. J., Bloch, W., Mehlhorn, U.
(2004). Myocardial apoptosis prevention by radical scavenging in patients undergoing cardiac surgery. J. Thorac. Cardiovasc. Surg.
128: 103-108
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Fan, G.-C., Chu, G., Mitton, B., Song, Q., Yuan, Q., Kranias, E. G.
(2004). Small Heat-Shock Protein Hsp20 Phosphorylation Inhibits {beta}-Agonist-Induced Cardiac Apoptosis. Circ. Res.
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Corbucci, G. G., Perrino, C., Donato, G., Ricchi, A., Lettieri, B., Troncone, G., Indolfi, C., Chiariello, M., Avvedimento, E. V.
(2004). Transient and reversible deoxyribonucleic acid damage in human left ventricle under controlled ischemia and reperfusion. J Am Coll Cardiol
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Cirillo, M., Amaducci, A., Brunelli, F., Dalla Tomba, M., Parrella, P., Tasca, G., Troise, G., Quaini, E.
(2004). Determinants of postinfarction remodeling affect outcome and left ventricular geometry after surgical treatment of ischemic cardiomyopathy. J. Thorac. Cardiovasc. Surg.
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Fu, Y.-C., Chi, C.-S., Yin, S.-C., Hwang, B., Chiu, Y.-T., Hsu, S.-L.
(2004). Norepinephrine induces apoptosis in neonatal rat cardiomyocytes through a reactive oxygen species-TNF{alpha}-caspase signaling pathway. Cardiovasc Res
62: 558-567
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Gustafsson, A. B., Tsai, J. G., Logue, S. E., Crow, M. T., Gottlieb, R. A.
(2004). Apoptosis Repressor with Caspase Recruitment Domain Protects against Cell Death by Interfering with Bax Activation. J. Biol. Chem.
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Aries, A., Paradis, P., Lefebvre, C., Schwartz, R. J., Nemer, M.
(2004). Essential role of GATA-4 in cell survival and drug-induced cardiotoxicity. Proc. Natl. Acad. Sci. USA
101: 6975-6980
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Sayk, F., Kruger, S., Bechtel, J.F. M., Feller, A. C., Sievers, H. H., Bartels, C.
(2004). Significant damage of the conduction system during cardioplegic arrest is due to necrosis not apoptosis. Eur. J. Cardiothorac. Surg.
25: 801-806
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Thatte, H. S., Rhee, J.-H., Zagarins, S. E., Treanor, P. R., Birjiniuk, V., Crittenden, M. D., Khuri, S. F.
(2004). Acidosis-induced apoptosis in human and porcine heart. Ann. Thorac. Surg.
77: 1376-1383
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Pang, J.-J., Xu, R.-K., Xu, X.-B., Cao, J.-M., Ni, C., Zhu, W.-L., Asotra, K., Chen, M.-C., Chen, C.
(2004). Hexarelin protects rat cardiomyocytes from angiotensin II-induced apoptosis in vitro. Am. J. Physiol. Heart Circ. Physiol.
286: H1063-H1069
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