From the Myocardial Biology Unit and Cardiovascular Division, Departments
of Medicine, Boston Medical Center, Boston Veterans Affairs Medical Center,
and Boston University School of Medicine, Boston, Mass.
Correspondence to Dr Wilson S. Colucci, Boston Medical Center, 88 E Newton St, Boston, MA 02118. E-mail wilson.colucci{at}bmc.org
Background—Myocardial sympathetic
activity is increased in heart failure. We tested the hypothesis that
norepinephrine (NE) stimulates apoptosis in adult
rat ventricular myocytes in vitro.
Methods and Results—Myocytes were exposed to NE alone (10
µmol/L), NE+propranolol (2 µmol/L), NE+prazosin
(0.1 µmol/L), or isoproterenol (ISO, 10 µmol/L) for 24
hours. NE and ISO decreased the number of viable myocytes by
Conclusions—NE, acting via the ß-adrenergic pathway, stimulates
apoptosis in adult rat cardiac myocytes in vitro. This effect
is mediated by protein kinase A and requires calcium entry via
voltage-dependent calcium channels. NE-stimulated apoptosis of
cardiac myocytes may contribute to the progression of myocardial
failure.
© 1998 American Heart Association, Inc.
Basic Science Reports
Norepinephrine Stimulates Apoptosis in Adult Rat Ventricular Myocytes by Activation of the ß-Adrenergic Pathway
35%.
This effect was completely blocked by the ß-adrenergic
antagonist propranolol but was not affected by
the 
1-adrenergic antagonist prazosin. NE
increased DNA laddering on agarose gel electrophoresis and increased
the percentage of cells that were stained by terminal
deoxynucleotidyl transferase–mediated nick
end-labeling from 5.8±1.0% to 21.0±2.3% (P<0.01;
n=4). NE likewise increased the percentage of apoptotic cells
with hypodiploid DNA content as assessed by flow cytometry from
7.8±0.7% to 16.7±2.2% (P<0.01; n=6), and this
effect was abolished by propranolol but not prazosin. ISO
and forskolin (10 µmol/L) mimicked the effect of NE, increasing
the percentage of apoptotic cells to 14.7±1.9% and
14.4±2.2%, respectively. NE-stimulated apoptosis was
abolished by the protein kinase A inhibitor H-89 (20
µmol/L) or the voltage-dependent calcium channel blockers diltiazem
and nifedipine.
Key Words: apoptosis • norepinephrine • receptors, adrenergic, beta • myocytes • calcium
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A. Igawa, T. Nozawa, N. Fujii, B.-i. Kato, H. Asanoi, and H. Inoue Long-term treatment with Low-Dose, but not High-Dose, guanethidine improves ventricular function and survival of rats with heart failure after myocardial infarction J. Am. Coll. Cardiol., August 6, 2003; 42(3): 541 - 548. [Abstract] [Full Text] [PDF]
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 On behalf of the MERIT-HF Study Group, H. L. White, R. A. de Boer, A. Maqbool, D. Greenwood, D. J. van Veldhuisen, R. Cuthbert, S. G. Ball, A. S. Hall, and A. J. Balmforth An evaluation of the beta-1 adrenergic receptor Arg389Gly polymorphism in individuals with heart failure: a MERIT-HF sub-study Eur J Heart Fail, August 1, 2003; 5(4): 463 - 468. [Abstract] [Full Text] [PDF]
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 M. Pareja, O. Sanchez, J. Lorita, M. Soley, and I. Ramirez Activated epidermal growth factor receptor (ErbB1) protects the heart against stress-induced injury in mice Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2003; 285(2): R455 - R462. [Abstract] [Full Text] [PDF]
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H. Tomita, M. Nazmy, K. Kajimoto, G. Yehia, C. A. Molina, and J. Sadoshima Inducible cAMP Early Repressor (ICER) Is a Negative-Feedback Regulator of Cardiac Hypertrophy and an Important Mediator of Cardiac Myocyte Apoptosis in Response to {beta}-Adrenergic Receptor Stimulation Circ. Res., July 11, 2003; 93(1): 12 - 22. [Abstract] [Full Text] [PDF]
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G. Li, Y. Xiao, J. L. Estrella, C. A. Ducsay, R. D. Gilbert, and L. Zhang Effect of Fetal Hypoxia on Heart Susceptibility to Ischemia and Reperfusion Injury in the Adult Rat Reproductive Sciences, July 1, 2003; 10(5): 265 - 274. [Abstract] [PDF]
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 Y. Xiang and B. K. Kobilka Myocyte Adrenoceptor Signaling Pathways Science, June 6, 2003; 300(5625): 1530 - 1532. [Abstract] [Full Text] [PDF]
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C. Communal, F. Huq, D. Lebeche, C. Mestel, J. K. Gwathmey, and R. J. Hajjar Decreased Efficiency of Adenovirus-Mediated Gene Transfer in Aging Cardiomyocytes Circulation, March 4, 2003; 107(8): 1170 - 1175. [Abstract] [Full Text] [PDF]
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V. G. Sharov, A. Todor, G. Suzuki, H. Morita, E. J. Tanhehco, and H. N. Sabbah Hypoxia, angiotensin-II, and norepinephrine mediated apoptosis is stimulus specific in canine failed cardiomyocytes: a role for p38 MAPK, Fas-L and cyclin D1 Eur J Heart Fail, March 1, 2003; 5(2): 121 - 129. [Abstract] [Full Text] [PDF]
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A. Remondino, S. H. Kwon, C. Communal, D. R. Pimentel, D. B. Sawyer, K. Singh, and W. S. Colucci {beta}-Adrenergic Receptor-Stimulated Apoptosis in Cardiac Myocytes Is Mediated by Reactive Oxygen Species/c-Jun NH2-Terminal Kinase-Dependent Activation of the Mitochondrial Pathway Circ. Res., February 7, 2003; 92(2): 136 - 138. [Abstract] [Full Text] [PDF]
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 T. Yeh Jr, A. S. Wechsler, L. Graham, K. E. Loesser, D. A. Sica, L. Wolfe, and E. R. Jakoi Central sympathetic blockade ameliorates brain death-induced cardiotoxicity and associated changes in myocardial gene expression J. Thorac. Cardiovasc. Surg., December 1, 2002; 124(6): 1087 - 1098. [Abstract] [Full Text]
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 D. S. Goldstein, D. Robertson, M. Esler, S. E. Straus, and G. Eisenhofer Dysautonomias: Clinical Disorders of the Autonomic Nervous System Ann Intern Med, November 5, 2002; 137(9): 753 - 763. [Abstract] [Full Text] [PDF]
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P. Chiari, V. Piriou, G. Hadour, C. Rodriguez, J. Loufouat, J.-J. Lehot, M. Ovize, and R. Ferrera Preservation of ischemia and isoflurane-induced preconditioning after brain death in rabbit hearts Am J Physiol Heart Circ Physiol, November 1, 2002; 283(5): H1769 - H1774. [Abstract] [Full Text] [PDF]
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C. Stamm, I. Friehs, D. B. Cowan, H. Cao-Danh, Y.-H. Choi, L. F. Duebener, F. X. McGowan, and P. J. del Nido Dopamine Treatment of Postischemic Contractile Dysfunction Rapidly Induces Calcium-Dependent Pro-Apoptotic Signaling Circulation, September 24, 2002; 106(12_suppl_1): I-290 - I-298. [Abstract] [Full Text] [PDF]
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C. Lavoie, J.-F. Mercier, A. Salahpour, D. Umapathy, A. Breit, L.-R. Villeneuve, W.-Z. Zhu, R.-P. Xiao, E. G. Lakatta, M. Bouvier, et al. beta 1/beta 2-Adrenergic Receptor Heterodimerization Regulates beta 2-Adrenergic Receptor Internalization and ERK Signaling Efficacy J. Biol. Chem., September 13, 2002; 277(38): 35402 - 35410. [Abstract] [Full Text] [PDF]
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J. D. Kilts, T. Akazawa, M. D. Richardson, and M. M. Kwatra Age Increases Cardiac Galpha i2 Expression, Resulting in Enhanced Coupling to G Protein-coupled Receptors J. Biol. Chem., August 16, 2002; 277(34): 31257 - 31262. [Abstract] [Full Text] [PDF]
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B. Yusta, J. Estall, and D. J. Drucker Glucagon-like Peptide-2 Receptor Activation Engages Bad and Glycogen Synthase Kinase-3 in a Protein Kinase A-dependent Manner and Prevents Apoptosis following Inhibition of Phosphatidylinositol 3-Kinase J. Biol. Chem., July 5, 2002; 277(28): 24896 - 24906. [Abstract] [Full Text] [PDF]
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J. T. Auman, F. J. Seidler, C. A. Tate, and T. A. Slotkin Are developing beta -adrenoceptors able to desensitize? Acute and chronic effects of beta -agonists in neonatal heart and liver Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2002; 283(1): R205 - R217. [Abstract] [Full Text] [PDF]
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C. Communal, M. Sumandea, P. de Tombe, J. Narula, R. J. Solaro, and R. J. Hajjar Functional consequences of caspase activation in cardiac myocytes PNAS, April 18, 2002; (2002) 92022999. [Abstract] [Full Text] [PDF]
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Y. Shizukuda, P. M. Buttrick, Y. Zou, I. Komuro, A. Yao, W. Zhu, S. Kudoh, Y. Hiroi, M. Shimoyama, H. Uozumi, et al. Isoprotrenol Activates Extracellular Signal-Regulated Protein Kinases in Cardiomyocytes Through Calcineurin Response Circulation, January 15, 2002; 105 (2): e9 - e9. [Full Text] [PDF]
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 M. Zaugg, M. C. Schaub, T. Pasch, and D. R. Spahn Modulation of {beta}-adrenergic receptor subtype activities in perioperative medicine: mechanisms and sites of action Br. J. Anaesth., January 1, 2002; 88(1): 101 - 123. [Abstract] [Full Text] [PDF]
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J. T. Auman, F. J. Seidler, C. A. Tate, and T. A. Slotkin beta -Adrenoceptor-mediated cell signaling in the neonatal heart and liver: responses to terbutaline Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2001; 281(6): R1895 - R1901. [Abstract] [Full Text] [PDF]
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M. A. Fortuno, S. Ravassa, A. Fortuno, G. Zalba, and J. Diez Cardiomyocyte Apoptotic Cell Death in Arterial Hypertension: Mechanisms and Potential Management Hypertension, December 1, 2001; 38(6): 1406 - 1412. [Abstract] [Full Text] [PDF]
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P. K. Tithof, M. Elgayyar, H. M. Schuller, M. Barnhill, and R. Andrews 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone, a nicotine derivative, induces apoptosis of endothelial cells Am J Physiol Heart Circ Physiol, November 1, 2001; 281(5): H1946 - H1954. [Abstract] [Full Text] [PDF]
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 R.-P. Xiao {beta}-Adrenergic Signaling in the Heart: Dual Coupling of the {beta}2-Adrenergic Receptor to Gs and Gi Proteins Sci. Signal., October 16, 2001; 2001(104): re15 - re15. [Abstract] [Full Text] [PDF]
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C. Maack, T. Elter, G. Nickenig, K. LaRosee, M. Crivaro, A. Stablein, H. Wuttke, and M. Bohm Prospective crossover comparison of carvedilol and metoprolol in patients with chronic heart failure J. Am. Coll. Cardiol., October 1, 2001; 38(4): 939 - 946. [Abstract] [Full Text] [PDF]
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J. T. Auman, F. J. Seidler, and T. A. Slotkin Regulation of fetal cardiac and hepatic beta -adrenoceptors and adenylyl cyclase signaling: terbutaline effects Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2001; 281(4): R1079 - R1089. [Abstract] [Full Text] [PDF]
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 H. E. Dincer, N. Gangopadhyay, R. Wang, and B. D. Uhal Norepinephrine induces alveolar epithelial apoptosis mediated by {alpha}-, {beta}-, and angiotensin receptor activation Am J Physiol Lung Cell Mol Physiol, September 1, 2001; 281(3): L624 - L630. [Abstract] [Full Text] [PDF]
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F. Qin, N. K. Rounds, W. Mao, K. Kawai, and C.-s. Liang Antioxidant vitamins prevent cardiomyocyte apoptosis produced by norepinephrine infusion in ferrets Cardiovasc Res, September 1, 2001; 51(4): 736 - 748. [Abstract] [Full Text] [PDF]
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 M. Henaff, S. N. Hatem, and J.-J. Mercadier Low Catecholamine Concentrations Protect Adult Rat Ventricular Myocytes against Apoptosis through cAMP-Dependent Extracellular Signal-Regulated Kinase Activation Mol. Pharmacol., April 13, 2001; 58(6): 1546 - 1553. [Abstract] [Full Text]
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F. Wang, Y. Seta, G. Baumgarten, D. J. Engel, N. Sivasubramanian, and D. L. Mann Functional Significance of Hemodynamic Overload-Induced Expression of Leukemia-Inhibitory Factor in the Adult Mammalian Heart Circulation, March 6, 2001; 103(9): 1296 - 1302. [Abstract] [Full Text] [PDF]
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 F. Farhat, D. Loisance, J.-P. Garnier, and M. Kirsch Norepinephrine release after acute brain death abolishes the cardioprotective effects of ischemic preconditioning in rabbit Eur. J. Cardiothorac. Surg., March 1, 2001; 19(3): 313 - 320. [Abstract] [Full Text] [PDF]
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W.-Z. Zhu, M. Zheng, W. J. Koch, R. J. Lefkowitz, B. K. Kobilka, and R.-P. Xiao Dual modulation of cell survival and cell death by beta 2-adrenergic signaling in adult mouse cardiac myocytes PNAS, February 13, 2001; 98(4): 1607 - 1612. [Abstract] [Full Text] [PDF]
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