Cited by 390Cell death mechanisms and regulationCardiomyopathy and Myosin StudiesCardiac Ischemia and Reperfusion

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Functional consequences of caspase activation in cardiac myocytes

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Communal, Catherine, Sumandea, Marius, de Tombe, Pieter, Narula, Jagat, Solaro, R. John, Hajjar, Roger J.·2002·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.092022999PMC PMC122935

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Abstract

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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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
ORCID: Solaro, R. John
Hajjar, Roger J.
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
DOI: 10.1073/pnas.092022999
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 › Cardiology and Cardiovascular 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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Functional consequences of caspase activation in cardiac myocytes

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