Functional consequences of caspase activation in cardiac myocytes
Open accessAbstract
Cardiomyocyte apoptosis is present in many cardiac disease states, including heart failure and ischemic heart disease. Apoptosis is associated with the activation of caspases that mediate the cleavage of vital and structural proteins. However, the functional contribution of apoptosis to these conditions is not known. Furthermore, in cardiac myocytes, apoptosis may not be complete, allowing the cells to persist for a prolonged period within the myocardium. Therefore, we examined whether caspase-3 cleaved cardiac myofibrillar proteins and, if so, whether it affects contractile function. The effects of caspase-3 were studied in vitro on individual components of the cardiac myofilament including α-actin, α-actinin, myosin heavy chain, myosin light chain 1/2, tropomyosin, cardiac troponins (T, I, C), and the trimeric troponin complex. Exposure of the myofibrillar protein (listed above) to caspase-3 for 4 h resulted in the cleavage of α-actin and α-actinin, but not myosin heavy chain, myosin light chain 1/2, and tropomyosin, into three fragments (30, 20, and 15 kDa) and one major fragment (45 kDa), respectively. When cTnT, cTnI, and cTnC were incubated individually with caspase-3, there was no detectable cleavage. However, when the recombinant troponin complex was exposed to caspase-3, cTnT was cleaved, resulting in fragments of 25 kDa. Furthermore, rat cardiac myofilaments exposed to caspase-3 exhibited similar patterns of myofibrillar protein cleavage. Treatment with the caspase inhibitor DEVD-CHO or z-VAD-fmk abolished the cleavage. Myofilaments, isolated from adult rat ventricular myocytes after induction of apoptotic pathway by using β-adrenergic stimulation, displayed a similar pattern of actin and TnT cleavage. Exposure of skinned fiber to caspase-3 decreased maximal Ca 2+ -activated force and myofibrillar ATPase activity. Our results indicate that caspase-3 cleaved myofibrillar proteins, resulting in an impaired force/Ca 2+ relationship and myofibrillar ATPase activity. Induction of apoptosis in cardiac cells was associated with similar cleavage of myofilaments. Therefore, activation of apoptotic pathways may lead to contractile dysfunction before cell death.
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Activation of several proteases in the apoptotic cascade can cleave various contractile proteins, leading to deterioration in contractile function of existing myocytes.
“Besides the obvious role of apoptotic cell death in myocyte loss, activation of several proteases in the apoptotic cascade can cleave various contractile proteins (α-actin, α-actinin, α, β-myosin heavy chain, tropomyosin and troponins, Ref. 56), leading to deterioration in contractile function of the existing myocytes.”
From Cardiac remodeling in obesity (2008) · cites this paper as [56]
Cites
Apoptosis in the Failing Human Heart
Olivetti, G., Abbi, R., Quaini, F., Kajstura, J., Cheng, W., Nitahara, J. A., Quaini, E., Di Loreto, C., Beltrami, C. A., Krajewski, S., et al. (1997) · New England Journal of Medicine · doi:10.1056/nejm199704173361603 · Cited by 1,673 · see citing works
Apoptosis in Myocytes in End-Stage Heart Failure
Narula, J., Haider, N., Virmani, R., DiSalvo, T. G., Kolodgie, F. D., Hajjar, R. J., Schmidt, U., Semigran, M. J., Dec, G. W., & Khaw, B.-A. (1996) · New England Journal of Medicine · doi:10.1056/nejm199610173351603 · Cited by 1,430 · see citing works
Self-citationCommunal, C., Singh, K., Pimentel, D. R., & Colucci, W. S. (1998) · Circulation · doi:10.1161/01.cir.98.13.1329 · Cited by 690 · see citing works
Self-citationNarula, J., Pandey, P., Arbustini, E., Haider, N., Narula, N., Kolodgie, F. D., Bello, B. D., Semigran, M. J., Bielsa-Masdeu, A., Dec, G. W., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.14.8144 · Cited by 586 · see citing works
Self-citationEvidence of Apoptosis in Arrhythmogenic Right Ventricular Dysplasia
Mallat, Z., Tedgui, A., Fontaliran, F., Frank, R., Durigon, M., & Fontaine, G. H. (1996) · New England Journal of Medicine · doi:10.1056/nejm199610173351604 · Cited by 415 · see citing works
Schwinger, R. H. G., Böhm, M., Schmidt, U., Karczewski, P., Bavendiek, U., Flesch, M., Krause, E.-G., & Erdmann, E. (1995) · Circulation · doi:10.1161/01.cir.92.11.3220 · Cited by 395 · see citing works
[22] Preparation of troponin and its subnits
Potter, J. D. (1982) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(82)85024-6 · Cited by 358 · see citing works
The role of the cytoskeleton in heart failure
Hein, S. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00268-0 · Cited by 354 · see citing works
Kanoh, M., Takemura, G., Misao, J., Hayakawa, Y., Aoyama, T., Nishigaki, K., Noda, T., Fujiwara, T., Fukuda, K., Minatoguchi, S., et al. (1999) · Circulation · doi:10.1161/01.cir.99.21.2757 · Cited by 321 · see citing works
Breakdown and Release of Myofilament Proteins During Ischemia and Ischemia/Reperfusion in Rat Hearts
Eyk, J. E. V., Powers, F. G., Law, W. R., Larue, C., Hodges, R. S., & Solaro, R. J. (1998) · Circulation Research · doi:10.1161/01.res.82.2.261 · Cited by 234 · see citing works
Self-citationProtein Kinase A Does Not Alter Economy of Force Maintenance in Skinned Rat Cardiac Trabeculae
de Tombe, P. P., & Stienen, G. J. M. (1995) · Circulation Research · doi:10.1161/01.res.76.5.734 · Cited by 141 · see citing works
Molecular genetic studies of familial hypertrophic cardiomyopathy
Seidman, C. E., & Seidman, J. G. (1998) · Basic Research in Cardiology · doi:10.1007/s003950050196 · Cited by 89 · see citing works
Hajjar, R. J., & Gwathmey, J. K. (1992) · Circulation · doi:10.1161/01.cir.86.6.1819 · Cited by 86 · see citing works
Self-citationMargossian, S. S., White, H. D., Caulfield, J., Norton, P. A., Taylor, S., & Slayter, H. S. (1992) · Circulation · doi:10.1161/01.cir.85.5.1720 · Cited by 86 · see citing works
Papp, Z. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00374-0 · Cited by 86 · see citing works
Ruetten, H., Badorff, C., Ihling, C. H., Zeiher, A. M., & Dimmeler, S. (2001) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(01)01670-9 · Cited by 77 · see citing works
Myofilament Calcium Regulation in Human Myocardium
Hajjar, R. J., Schwinger, R. H. G., Schmidt, U. H., Kim, C. S., Lebeche, D., Doye, A. A., & Gwathmey, J. K. (2000) · Circulation · doi:10.1161/01.cir.101.14.1679 · Cited by 55 · see citing works
Self-citationTroponin I, Stunning, Hypertrophy, and Failure of the Heart
Solaro, R. J. (1999) · Circulation Research · doi:10.1161/01.res.84.1.122 · Cited by 55 · see citing works
Self-citationManipulating the Contractile Apparatus: Genetically Defined Animal Models of Cardiovascular Disease
Dalloz, F., Osińska, H. E., & Robbins, J. M. (2001) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1289 · Cited by 37 · see citing works
Brixius, K., Mehlhorn, U., Bloch, W., & Schwinger, R. H. (2000) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39031-7 · Cited by 30 · see citing works
Münch, G., Bölck, B., Sugaru, A., Brixius, K., Bloch, W., & Schwinger, R. H. G. (2001) · Circulation · doi:10.1161/01.cir.103.22.2739 · Cited by 24 · see citing works
SERCA2a activity correlates with the force-frequency relationship in human myocardium
Münch, G., Bölck, B., Brixius, K., Reuter, H., Mehlhorn, U., Bloch, W., & Schwinger, R. H. G. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.278.6.h1924 · Cited by 23 · see citing works
A mouse model of myocardial stunning
Murphy, A. M., Kögler, H., & Marbán, E. (2000) · Molecular Medicine Today · doi:10.1016/s1357-4310(00)01732-9 · Cited by 9 · see citing works
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Apoptosis: controlled demolition at the cellular level
Taylor, R. C., Cullen, S. P., & Martin, S. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2312 · Cited by 2,617 · see citing works
Many cuts to ruin: a comprehensive update of caspase substrates
Fischer, U., Jänicke, R. U., & Schulze‐Osthoff, K. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401160 · Cited by 1,025 · see citing works
Fundamental Mechanisms of Regulated Cell Death and Implications for Heart Disease
Re, D. P. D., Amgalan, D., Linkermann, A., Liu, Q., & Kitsis, R. N. (2019) · Physiological Reviews · doi:10.1152/physrev.00022.2018 · Cited by 979 · see citing works
A mechanistic role for cardiac myocyte apoptosis in heart failure
Wencker, D., Chandra, M., Nguyen, K., Miao, W., Garantziotis, S., Factor, S. M., Shirani, J., Armstrong, R. C., & Kitsis, R. N. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17664 · Cited by 765 · see citing works
Cell Death in the Pathogenesis of Heart Disease: Mechanisms and Significance
Whelan, R. S., Kaplinskiy, V., & Kitsis, R. N. (2010) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163111 · Cited by 751 · see citing works
Abel, E. D., Litwin, S. E., & Sweeney, G. (2008) · Physiological Reviews · doi:10.1152/physrev.00017.2007 · Cited by 736 · see citing works
Fluorogenic probes for disease-relevant enzymes
Zhang, J., Chai, X., He, X., Kim, H.-J., Yoon, J., & Tian, H. (2018) · Chemical Society Reviews · doi:10.1039/c7cs00907k · Cited by 606 · see citing works
Myocytes Die by Multiple Mechanisms in Failing Human Hearts
Kostin, S., Pool, L., Elsässer, A., Hein, S., Drexler, H. C. A., Arnon, E., Hayakawa, Y., Zimmermann, R., Bauer, E., Klövekorn, W.-P., et al. (2003) · Circulation Research · doi:10.1161/01.res.0000067471.95890.5c · Cited by 564 · see citing works
Cardoso, A. L., Fernandes, A. M. A., Aguilar‐Pimentel, J. A., de Angelis, M. H., Guedes, J. R., Brito, M. A., Ortolano, S., Pani, G., Athanasopoulou, S., Gonos, E. S., et al. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.07.004 · Cited by 471 · see citing works
Myocyte apoptosis in heart failure
VANEMPEL, V., Bertrand, A., Hofstra, L., Crijns, H. J. G. M., Doevendans, P. A., & Windt, L. J. D. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.04.012 · Cited by 374 · see citing works
Apoptotic and non-apoptotic programmed cardiomyocyte death in ventricular remodelling
Dorn, G. W. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn243 · Cited by 301 · see citing works
Anthracyclines Induce Calpain-dependent Titin Proteolysis and Necrosis in Cardiomyocytes
Lim, C. C., Zuppinger, C., Guo, X., Kuster, G. M., Helmes, M., Eppenberger, H. M., Suter, T. M., Liao, R., & Sawyer, D. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m308033200 · Cited by 303 · see citing works
Cauwe, B., & Opdenakker, G. (2010) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2010.501783 · Cited by 296 · see citing works
Haudek, S. B., Taffet, G. E., Schneider, M. D., & Mann, D. L. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29134 · Cited by 277 · see citing works
Matsui, T., & Rosenzweig, A. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.11.005 · Cited by 263 · see citing works
Degradation of Myosin Light Chain in Isolated Rat Hearts Subjected to Ischemia-Reperfusion Injury
Sawicki, G., León, H., Sawicka, J., Sarıahmetoğlu, M., Schulze, C. J., Scott, P. G., Szczesna‐Cordary, D., & Schulz, R. (2005) · Circulation · doi:10.1161/circulationaha.104.531616 · Cited by 263 · see citing works
Mechanisms of Atrial Fibrillation: Lessons From Animal Models
Nattel, S., Shiroshita-Takeshita, A., Brundel, B. J. J. M., & Rivard, L. (2005) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2005.06.002 · Cited by 243 · see citing works
Hayakawa, Y., Chandra, M., Miao, W., Shirani, J., Brown, J. H., Dorn, G. W., Armstrong, R. C., & Kitsis, R. N. (2003) · Circulation · doi:10.1161/01.cir.0000101920.72665.58 · Cited by 222 · see citing works
TNNT1, TNNT2, and TNNT3: Isoform genes, regulation, and structure–function relationships
Wei, B. K., & Jin, J. (2016) · Gene · doi:10.1016/j.gene.2016.01.006 · Cited by 222 · see citing works
Pathophysiology of sepsis-induced myocardial dysfunction
Lv, X., & Wang, H. (2016) · Military Medical Research · doi:10.1186/s40779-016-0099-9 · Cited by 220 · see citing works
Chang, H., Shin, M., Yang, H.-Y., Lee, J. W., Kim, Y., Lee, M., Kim, J., Kim, K. H., & Kim, C. (2006) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.29.1597 · Cited by 215 · see citing works
ER stress contributes to ischemia-induced cardiomyocyte apoptosis
Szegezdi, É., Duffy, A. M., O’Mahoney, M. E., Logue, S. E., Mylotte, L. A., O’Brien, T., & Afshin Samali, A. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.09.009 · Cited by 197 · see citing works
Oxidative Stress and Sarcomeric Proteins
Steinberg, S. F. (2013) · Circulation Research · doi:10.1161/circresaha.111.300496 · Cited by 195 · see citing works
Cardiovascular effects of leptin
Sweeney, G. (2009) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2009.224 · Cited by 184 · see citing works
Sumandea, M. P., Pyle, W. G., Kobayashi, T., de Tombe, P. P., & Solaro, R. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306325200 · Cited by 182 · see citing works
Self-citationRoy, A. M., Baliga, M. S., & Katiyar, S. K. (2005) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.81.4.1 · Cited by 168 · see citing works
Nebigil, C. G., Étienne-Selloum, N., Messaddeq, N., & Maroteaux, L. (2003) · The FASEB Journal · doi:10.1096/fj.02-1122fje · Cited by 155 · see citing works
MitoQ administration prevents endotoxin-induced cardiac dysfunction
Supinski, G. S., Murphy, M. P., & Callahan, L. A. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90902.2008 · Cited by 152 · see citing works
Induction of apoptosis by caffeine is mediated by the p53, Bax, and caspase 3 pathways.
He, Z., Ma, W.-Y., Hashimoto, T., Bode, A. M., Yang, C. S., & Dong, Z. (2003) · PubMed · Cited by 152 · see citing works
Chandrashekhar, Y., Sen, S., Anway, R., Shuros, A., & Anand, I. (2004) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2003.09.026 · Cited by 149 · see citing works
Troponin T isoforms and posttranscriptional modifications: Evolution, regulation and function
Wei, B. K., & Jin, J. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.10.013 · Cited by 146 · see citing works
Laufer, E. M., Mingels, A. M. A., Winkens, M. H. M., Joosen, I. A., Schellings, M. W. M., Leiner, T., Wildberger, J. E., Narula, J., van Dieijen‐Visser, M. P., & Hofstra, L. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.200394 · Cited by 144 · see citing works
Self-citationMechanisms of Disease: apoptosis in heart failure—seeing hope in death
Narula, J., Haider, N., Arbustini, E., & Chandrashekhar, Y. (2006) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio0710 · Cited by 143 · see citing works
Self-citationCardiomyocyte apoptosis in hypertensive cardiomyopathy
González, A. (2003) · Cardiovascular Research · doi:10.1016/s0008-6363(03)00498-x · Cited by 138 · see citing works
Tiburcy, M., Didié, M., Boy, O., Christalla, P., Döker, S., Naito, H., Karikkineth, B. C., El‐Armouche, A., Grimm, M. F., Nose, M., et al. (2011) · Circulation Research · doi:10.1161/circresaha.111.251843 · Cited by 137 · see citing works
Mechanisms of Apoptosis in the Heart
Gustafsson, Å. B., & Gottlieb, R. (2003) · Journal of Clinical Immunology · doi:10.1023/b:joci.0000010421.56035.60 · Cited by 154 · see citing works
Ventricular Myocyte Caspases Are Directly Responsible for Endotoxin-Induced Cardiac Dysfunction
Lancel, S., Joulin, O., Favory, R., Goossens, J. F., Kluza, J., Chopin, C., Formstecher, P., Marchetti, P., & Nevière, R. (2005) · Circulation · doi:10.1161/circulationaha.104.490979 · Cited by 127 · see citing works
Chai, R., Fu, H., Zheng, Z., Liu, T., Ji, S., & Li, G. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7612 · Cited by 127 · see citing works
Neuroglobin and cytoglobin expression in mice
Fordel, E., Thijs, L., Moens, L. J., & Dewilde, S. (2007) · FEBS Journal · doi:10.1111/j.1742-4658.2007.05679.x · Cited by 126 · see citing works
Brundel, B. J. J. M., Henning, R. H., Ke, L., Gelder, I. C. V., Crijns, H. J. G. M., & Kampinga, H. H. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.06.068 · Cited by 124 · see citing works
van Empel, V. P. M., Bertrand, A., van der Nagel, R., Sawa Kostin, D., Doevendans, P. A., Crijns, H. J. G. M., de Wit, E., Sluiter, W. J., Ackerman, S. L., & Windt, L. J. D. (2005) · Circulation Research · doi:10.1161/01.res.0000172081.30327.28 · Cited by 121 · see citing works
Endotoxin-Induced Myocardial Dysfunction
Chagnon, F., Metz, C. N., Bucala, R., & Lesur, O. (2005) · Circulation Research · doi:10.1161/01.res.0000168327.22888.4d · Cited by 118 · see citing works
Anastasis: recovery from the brink of cell death
Tang, H. M., & Tang, H. L. (2018) · Royal Society Open Science · doi:10.1098/rsos.180442 · Cited by 117 · see citing works
Involvement of mitogen-activated protein kinases in adriamycin-induced cardiomyopathy
Lou, H., Danelisen, I., & Singal, P. K. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01054.2004 · Cited by 115 · see citing works
Reeve, J. L. V., Duffy, A. M., O'Brien, T., & Samali, A. (2005) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2005.tb00492.x · Cited by 113 · see citing works
Tumor necrosis factor-α-induced caspase activation mediates endotoxin-related cardiac dysfunction*
Carlson, D., Willis, M. S., White, D. J., Horton, J. W., & Giroir, B. P. (2005) · Critical Care Medicine · doi:10.1097/01.ccm.0000163398.79679.66 · Cited by 113 · see citing works
Rodrigo, R., Prieto, J. C., & Castillo, R. L. (2012) · Clinical Science · doi:10.1042/cs20110663 · Cited by 111 · see citing works
Atrial Fibrillation: Basic Mechanisms, Remodeling and Triggers
Shiroshita-Takeshita, A., Brundel, B. J. J. M., & Nattel, S. (2005) · Journal of Interventional Cardiac Electrophysiology · doi:10.1007/s10840-005-2362-y · Cited by 107 · see citing works
Essential myosin light chain as a target for caspase-3 in failing myocardium
Moretti, A., Weig, H., Ott, T., Seyfarth, M., Holthoff, H., Grewe, D., Gillitzer, A., Bott‐Flügel, L., Schömig, A., Ungerer, M., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182373099 · Cited by 106 · see citing works
Movassagh, M., & Foo, R. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9070-x · Cited by 106 · see citing works
Whidden, M. A., McClung, J. M., Falk, D. J., Hudson, M. B., Smuder, A. J., Nelson, W. B., & Powers, S. K. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91106.2008 · Cited by 105 · see citing works
Time-Dependent Degradation Pattern of Cardiac Troponin T Following Myocardial Infarction
Cardinaels, E. P. M., Mingels, A. M. A., van Rooij, T., Collinson, P. O., Prinzen, F. W., & van Dieijen‐Visser, M. P. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.200543 · Cited by 105 · see citing works
Grape Seed Proanthocyanidins Induce Apoptosis through p53, Bax, and Caspase 3 Pathways
Roy, A. M., Baliga, M. S., Elmets, C. A., & Katiyar, S. K. (2005) · Neoplasia · doi:10.1593/neo.04412 · Cited by 104 · see citing works
Apoptosis and heart failure: clinical relevance and therapeutic target
GARG, S., NARULA, J., & CHANDRASHEKHAR, Y. (2005) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.11.006 · Cited by 103 · see citing works
Self-citationRole of various proteases in cardiac remodeling and progression of heart failure
Muller, A. L., & Dhalla, N. S. (2011) · Heart Failure Reviews · doi:10.1007/s10741-011-9269-8 · Cited by 99 · see citing works
Wang, X., Wang, Q., Guo, W., & Zhu, Y. Z. (2010) · Bioscience Reports · doi:10.1042/bsr20100003 · Cited by 96 · see citing works
Caspase-3 as a therapeutic target for heart failure
Yang, B., Ye, D., & Wang, Y. (2013) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2013.745513 · Cited by 96 · see citing works
Samengo, G., Avik, A., Fedor, B., Whittaker, D., Myung, K. H., Wehling‐Henricks, M., & Tidball, J. G. (2012) · Aging Cell · doi:10.1111/acel.12003 · Cited by 95 · see citing works
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Balakumar, P., & Jagadeesh, G. (2010) · Pharmacological Research · doi:10.1016/j.phrs.2010.07.003 · Cited by 94 · see citing works
Zhang, Z., Biesiadecki, B. J., & Jin, J. (2006) · Biochemistry · doi:10.1021/bi060273s · Cited by 94 · see citing works
Brennan, C. M., Emerson, C. P., Owens, J. M., & Christoforou, N. (2021) · JCI Insight · doi:10.1172/jci.insight.149915 · Cited by 92 · see citing works
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Beeri, R., Yosefy, C., Guerrero, J., Delling, F. N., Abedat, S., Chaput, M., del Monte, F., Handschumacher, M. D., Stroud, R. E., Sullivan, S. M., et al. (2008) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2007.07.093 · Cited by 90 · see citing works
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Nebigil, C. G. (2001) · Trends in Cardiovascular Medicine · doi:10.1016/s1050-1738(01)00135-9 · Cited by 90 · see citing works
Vahebi, S., Ota, A., Li, M., Warren, C. M., de Tombe, P. P., Wang, Y., & Solaro, R. J. (2007) · Circulation Research · doi:10.1161/01.res.0000258116.60404.ad · Cited by 89 · see citing works
Self-citationRadhakrishnan, J., Wang, S., Ayoub, I. M., Kolarova, J. D., Levine, R. F., & Gazmuri, R. J. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00468.2006 · Cited by 89 · see citing works
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Supinski, G. S., & Callahan, L. A. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01288.2005 · Cited by 89 · see citing works
Chen, F. C., & Ogut, O. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00419.2005 · Cited by 88 · see citing works
Jayasankar, V., Woo, Y.-P. J., Pirolli, T. J., Bish, L. T., Berry, M. F., Burdick, J., Gardner, T. J., & Sweeney, H. L. (2005) · Journal of Cardiac Surgery · doi:10.1111/j.0886-0440.2005.200373.x · Cited by 88 · see citing works
Calpain mediates cardiac troponin degradation and contractile dysfunction in atrial fibrillation
Ke, L., Qi, X. Y., Dijkhuis, A., Chartier, D., Nattel, S., Henning, R. H., Kampinga, H. H., & Brundel, B. J. J. M. (2008) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2008.08.012 · Cited by 86 · see citing works
Xu, W., Liu, J., Liu, H.-K., Qi, G.-Y., Sun, X., Sun, W., & Chen, B. (2009) · Nutrition · doi:10.1016/j.nut.2008.10.019 · Cited by 86 · see citing works
Modulation of Thin Filament Activation by Breakdown or Isoform Switching of Thin Filament Proteins
Marston, S. B., & Redwood, C. S. (2003) · Circulation Research · doi:10.1161/01.res.0000105088.06696.17 · Cited by 86 · see citing works
Myofibrillar remodelling in cardiac hypertrophy, heart failure and cardiomyopathies
Macháčková, J., Barta, J., & Dhalla, N. S. (2006) · Canadian Journal of Cardiology · doi:10.1016/s0828-282x(06)70315-4 · Cited by 84 · see citing works
González‐Juanatey, J. R., Iglesias, M. J., Alcaide, C., Piñeiro, R., & Lago, F. (2003) · Circulation · doi:10.1161/01.cir.0000043803.20822.d1 · Cited by 84 · see citing works
Adamy, C., Mulder, P. G. H., Khouzami, L., Andrieu‐Abadie, N., Defer, N., Candiani, G., Pavoine, C., Caramelle, P., Souktani, R., Corvoisier, P. L., et al. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.06.010 · Cited by 83 · see citing works
Neuregulin-1 attenuated doxorubicin-induced decrease in cardiac troponins
Bian, Y., Sun, M., Silver, M., Ho, K. K. L., Marchionni, M. A., Caggiano, A. O., Stone, J. R., Amende, I., Hampton, T., Morgan, J. P., et al. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01010.2008 · Cited by 82 · see citing works
Inserte, J. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.06.001 · Cited by 81 · see citing works
Brundel, B. J. J. M. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.02.007 · Cited by 79 · see citing works
Trent, J. C., Patel, S. S., Zhang, J., Araujo, D. M., Plana, J., Lenihan, D. J., Fan, D., PATEL, S. R., Benjamin, R. S., & Khakoo, A. Y. (2009) · Cancer · doi:10.1002/cncr.24683 · Cited by 77 · see citing works
Scarabelli, T. M., & Gottlieb, R. A. (2004) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401544 · Cited by 77 · see citing works
Clinical Implications of Apoptosis in Ischemic Myocardium
Scarabelli, T. M., Knight, R. A., Stephanou, A., Townsend, P. A., Chen-Scarabelli, C. A., Lawrence, K. M., Gottlieb, R. A., Latchman, D. S., & Narula, J. (2006) · Current Problems in Cardiology · doi:10.1016/j.cpcardiol.2005.11.002 · Cited by 76 · see citing works
Self-citationFeng, H., Biesiadecki, B. J., Yu, Z., Hossain, M. M., & Jin, J. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.153577 · Cited by 75 · see citing works
Molecular and Integrated Biology of Thin Filament Protein Phosphorylation in Heart Muscle
Sumandea, M. P., Burkart, E. M., Kobayashi, T., de Tombe, P. P., & Solaro, R. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1302.004 · Cited by 75 · see citing works
Self-citationNoninvasive Detection of Programmed Cell Loss with 99mTc-Labeled Annexin A5 in Heart Failure
Kietselaer, B., Reutelingsperger, C. P. M., Boersma, H. H., Heidendal, G. A. K., Liem, I. H., Crijns, H. J. G. M., Narula, J., & Hofstra, L. (2007) · Journal of Nuclear Medicine · doi:10.2967/jnumed.106.039453 · Cited by 74 · see citing works
Self-citationThe Anticancer Activities of Wogonin in Murine Sarcoma S180 both in Vitro and in Vivo
Wang, W., Guo, Q., You, Q., Zhang, K., Yang, Y., Yu, J., Liu, W., Zhao, L., Gu, H.-Y., Hu, Y., et al. (2006) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.29.1132 · Cited by 71 · see citing works
Lee, Y., Cheng, P.-Y., Chim, L.-S., Kung, C.-W., Ka, S., Chung, M.-T., & Sheu, J. (2011) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2011.03.009 · Cited by 71 · see citing works
Leptin attenuates cardiac apoptosis after chronic ischaemic injury
McGaffin, K. R., Zou, B., McTiernan, C. F., & O'Donnell, C. P. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp071 · Cited by 71 · see citing works
Intrinsic-mediated caspase activation is essential for cardiomyocyte hypertrophy
Putinski, C., Abdul‐Ghani, M., Stiles, R., Brunette, S., Dick, S. A., Fernando, P., & Megeney, L. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315587110 · Cited by 71 · see citing works
Modeling Human Cardiac Hypertrophy in Stem Cell-Derived Cardiomyocytes
Ovchinnikova, E. S., Hoes, M. F., Ustyantsev, K., Bömer, N., de Jong, T. V., van der Mei, H. C., Berezikov, E., & van der Meer, P. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.01.016 · Cited by 69 · see citing works
Yun, J., & Lee, D. G. (2016) · IUBMB Life · doi:10.1002/iub.1527 · Cited by 70 · see citing works
High-Sensitivity Troponin T Level and Angiographic Severity of Coronary Artery Disease
Ndrepepa, G., Braun, S., Schulz, S., Mehilli, J., Schömig, A., & Kastrati, A. (2011) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2011.04.012 · Cited by 69 · see citing works
Molecular Basis of Cardioprotective Effect of Antioxidant Vitamins in Myocardial Infarction
Rodrigo, R., Libuy, M., Feliú, F., & Hasson, D. (2013) · BioMed Research International · doi:10.1155/2013/437613 · Cited by 68 · see citing works
Significance and interpretation of elevated troponin in septic patients.
Favory, R., & Nevière, R. (2006) · Critical Care · doi:10.1186/cc4991 · Cited by 67 · see citing works
Cardiomyocyte-specific disruption of Cathepsin K protects against doxorubicin-induced cardiotoxicity
Guo, R., Hua, Y., Ren, J. T., Bornfeldt, K., & Nair, S. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0727-2 · Cited by 66 · see citing works
Role of proteases in the pathophysiology of cardiac disease
Singh, R. B., Dandekar, S., Elimban, V., Gupta, S. K., & Dhalla, N. S. (2004) · Molecular and Cellular Biochemistry · doi:10.1023/b:mcbi.0000041865.63445.40 · Cited by 64 · see citing works
Functional Consequence of Serotonin/5-HT 2B Receptor Signaling in Heart
Nebigil, C. G., & Maroteaux, L. (2003) · Circulation · doi:10.1161/01.cir.0000081520.25714.d9 · Cited by 65 · see citing works
Sabri, A., Alcott, S., Elouardighi, H., Pak, E. S., Derian, C. K., Andrade‐Gordon, P., Kinnally, K. W., & Steinberg, S. F. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302718200 · Cited by 64 · see citing works
Yeh, C., Chen, T.-P., Lee, C.-H., Wu, Y., Lin, Y., & Lin, P. J. (2006) · Shock · doi:10.1097/01.shk.0000225863.56714.96 · Cited by 63 · see citing works
Sheng, J., & Jin, J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00165 · Cited by 62 · see citing works
Plassmeyer, M. L., Alpan, O., Corley, M. J., Premeaux, T. A., Lillard, K., Coatney, P., Vaziri, T., Michalsky, S., Pang, A. P. S., Bukhari, Z., et al. (2021) · Allergy · doi:10.1111/all.14907 · Cited by 61 · see citing works
Heat shock proteins as molecular targets for intervention in atrial fibrillation
Brundel, B. J. J. M., Ke, L., Dijkhuis, A., Qi, X., Shiroshita-Takeshita, A., Nattel, S., Henning, R. H., & Kampinga, H. H. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn060 · Cited by 61 · see citing works
- Authors
- Communal, C., Sumandea, M., de Tombe, P., Narula, J., Solaro, R. J., & Hajjar, R. J.
- Affiliations
- Harvard University (US)
- Cardiovascular Research Center, Massachusetts General Hospital, Charlestown, MA 02129; Harvard Medical School, Boston, MA 02115; Department of Physiology and Biophysics, University of Illinois, Chicago, IL 60612; and Division of Cardiology, Medical College of Pennsylvania/Hanehmann, Philadelphia, PA 19102
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2002-04-23
- Volume
- 99
- Issue
- 9
- Pages
- 6252-6256
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC122935
- OpenAlex
- W2016568695
- Cited by
- 390
- References
- 23
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 6 · 2023: 7 · 2022: 10 · 2021: 10 · 2020: 10 · 2019: 7 · 2018: 18 · 2017: 9 · 2016: 15 · 2015: 13 · 2014: 17 · 2013: 18 · 2012: 17
- FWCI
- 8.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (HL‐62426)
- U.S. Public Health Service (R01-63704)
- National Heart, Lung, and Blood Institute (HL61557, HL-57623, F32HL010409, P01 HL 62426, F32HL10409-02, R01HL061557, P01HL062426)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiomyopathy and Myosin Studies
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Keywords
- caspase-3, cardiomyocyte apoptosis, troponin T, troponin complex, cardiac contractile function, myofibrillar ATPase activity, calcium-activated force, beta-adrenergic stimulation, heart failure, ischemic heart disease, DEVD-CHO, z-VAD-fmk, ventricular myocytes
- MeSH terms
- Actinin, Actins, Adenosine Triphosphatases, Amino Acid Sequence, Animals, Cattle, Cells, Cultured, Electrophoresis, Polyacrylamide Gel, Enzyme Activation, Humans, Male, Molecular Sequence Data, Myocardium, Rabbits, Recombinant Proteins, Substrate Specificity, Time Factors, Tropomyosin, Troponin, Blotting, Western, Rats, Sprague-Dawley, Myosin Light Chains, Myosin Heavy Chains, Protein Isoforms, Caspases, Rats, Caspase 3
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