A cardiac mitochondrial cAMP signaling pathway regulates calcium accumulation, permeability transition and cell death
Open accessAbstract
Although cardiac cytosolic cyclic 3′,5′-adenosine monophosphate (cAMP) regulates multiple processes, such as beating, contractility, metabolism and apoptosis, little is known yet on the role of this second messenger within cardiac mitochondria. Using cellular and subcellular approaches, we demonstrate here the local expression of several actors of cAMP signaling within cardiac mitochondria, namely a truncated form of soluble AC (sAC t) and the exchange protein directly activated by cAMP 1 (Epac1), and show a protective role for sAC t against cell death, apoptosis as well as necrosis in primary cardiomyocytes. Upon stimulation with bicarbonate (HCO 3−) and Ca 2+, sAC t produces cAMP, which in turn stimulates oxygen consumption, increases the mitochondrial membrane potential (ΔΨm) and ATP production. cAMP is rate limiting for matrix Ca 2+ entry via Epac1 and the mitochondrial calcium uniporter and, as a consequence, prevents mitochondrial permeability transition (MPT). The mitochondrial cAMP effects involve neither protein kinase A, Epac2 nor the mitochondrial Na+/Ca 2+ exchanger. In addition, in mitochondria isolated from failing rat hearts, stimulation of the mitochondrial cAMP pathway by HCO 3− rescued the sensitization of mitochondria to Ca 2+-induced MPT. Thus, our study identifies a link between mitochondrial cAMP, mitochondrial metabolism and cell death in the heart, which is independent of cytosolic cAMP signaling. Our results might have implications for therapeutic prevention of cell death in cardiac pathologies.
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EPAC1 activation with bicarbonate decreases mitochondrial Ca2+ uptake, stimulates ATP production, and inhibits multiple forms of RCD including MPT-driven necrosis in rat cardiomyocytes.
“However, EPAC1 activation with bicarbonate reportedly decreases mitochondrial Ca2+ uptake, stimulates ATP production, and inhibits multiple forms of RCD including MPT-driven necrosis in rat cardiomyocytes [422].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [422]
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- Authors
- Wang, Z., Liu, D., Varin, A., Nicolas, V, Courilleau, D., Mateo, P., Caubere, C., Rouet, P., Gomez, A.-M., Vandecasteele, G., Fischmeister, R., & Brenner, C.
- Affiliations
- Université Paris-Sud (FR)
- Université Toulouse III - Paul Sabatier (FR)
- Corresponding author
- Brenner, C
- Venue
- Cell Death & Disease
- Published
- 2016-04-21
- Volume
- 7
- Issue
- 4
- Pages
- e2198-e2198
- ISSN
- 2041-4889 (ISSN-L)
- PMC
- PMC4855650
- OpenAlex
- W2338813507
- Cited by
- 106
- References
- 63
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 9 · 2023: 7 · 2022: 10 · 2021: 8 · 2020: 10 · 2019: 20 · 2018: 17 · 2017: 15 · 2016: 2
- FWCI
- 9.36
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Cell Death and Disease (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-11 IDEX-0003-01, ANR-13-ISV1-0001, ANR-11-IDEX-0003, ANR-11-IDEX, ANR-10, ANR-10-LABX, ANR-10-LABX-0033)
- Institut National de la Santé et de la Recherche Médicale (ANR-11-IDEX-0003-01)
- China Scholarship Council
- Institut National de la Recherche Agronomique
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Phosphodiesterase function and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- heart mitochondria, cAMP signaling, soluble adenylyl cyclase, Epac1, mitochondrial permeability transition, mitochondrial calcium uniporter, mitochondrial calcium accumulation, cardiomyocyte apoptosis, necrosis, mitochondrial membrane potential, ATP production, bicarbonate, heart failure, cardioprotection
- MeSH terms
- Cyclic AMP, Adenylyl Cyclases, Animals, Bicarbonates, Calcium, Camptothecin, Cells, Cultured, Dactinomycin, Heart Ventricles, Hydrogen Peroxide, Male, Mitochondria, Heart, Permeability, Signal Transduction, Rats, Wistar, Apoptosis, Troponin I, Guanine Nucleotide Exchange Factors, Myocytes, Cardiac, Rats, Membrane Potential, Mitochondrial
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