Rapid frequency-dependent changes in free mitochondrial calcium concentration in rat cardiac myocytes
Open accessAbstract
Key points Calcium ions regulate mitochondrial ATP production and contractile activity and thus play a pivotal role in matching energy supply and demand in cardiac muscle. The magnitude and kinetics of the changes in free mitochondrial calcium concentration in cardiac myocytes are largely unknown. Rapid stimulation frequency‐dependent increases but relatively slow decreases in free mitochondrial calcium concentration were observed in rat cardiac myocytes. This asymmetry caused a rise in the mitochondrial calcium concentration with stimulation frequency. These results provide insight into the mechanisms of mitochondrial calcium uptake and release that are important in healthy and diseased myocardium. Abstract Calcium ions regulate mitochondrial ATP production and contractile activity and thus play a pivotal role in matching energy supply and demand in cardiac muscle. Little is known about the magnitude and kinetics of the changes in free mitochondrial calcium concentration in cardiomyocytes. Using adenoviral infection, a ratiometric mitochondrially targeted Förster resonance energy transfer (FRET)‐based calcium indicator (4mtD3cpv, MitoCam) was expressed in cultured adult rat cardiomyocytes and the free mitochondrial calcium concentration ([Ca2+]m) was measured at different stimulation frequencies (0.1–4 Hz) and external calcium concentrations (1.8–3.6 mm) at 37°C. Cytosolic calcium concentrations were assessed under the same experimental conditions in separate experiments using Fura‐4AM. The increases in [Ca2+]m during electrical stimulation at 0.1 Hz were rapid (rise time = 49 ± 2 ms), while the decreases in [Ca2+]m occurred more slowly (decay half time = 1.17 ± 0.07 s). Model calculations confirmed that this asymmetry caused the rise in [Ca2+]m during diastole observed at elevated stimulation frequencies. Inhibition of the mitochondrial sodium–calcium exchanger (mNCE) resulted in a rise in [Ca2+]m at baseline and, paradoxically, in an acceleration of Ca2+ release. In conclusion: rapid increases in [Ca2+]m allow for fast adjustment of mitochondrial ATP production to increases in myocardial demand on a beat‐to‐beat basis and mitochondrial calcium release depends on mNCE activity and mitochondrial calcium buffering.
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Contraction-induced calcium uptake acutely increases OXPHOS and augments glucose transport and stimulates lipid uptake and oxidation through MEF2-induced expression of GLUT4 and PGC1α, respectively.
“Contraction-induced calcium uptake acutely increases OXPHOS (94, 177) and augments glucose transport and stimulates lipid uptake and oxidation through MEF2-induced expression of GLUT4 and PGC1α, respectively.”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [177]
Cites
Control of inositol 1,4,5-trisphosphate-induced Ca2+ release by cytosolic Ca2+
Bootman, M. D., Missiaen, L., Parys, J. B., SMEDT, H. D., & Casteels, R. (1995) · Biochemical Journal · doi:10.1042/bj3060445 · Cited by 5,120 · see citing works
Cardiac excitation–contraction coupling
Bers, D., & Despa, S. (2002) · Nature · doi:10.1038/415198a · Cited by 4,927 · see citing works
Mechanisms by which mitochondria transport calcium
Gunter, T. E., & Pfeiffer, D. R. (1990) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1990.258.5.c755 · Cited by 1,640 · see citing works
Regulation of mitochondrial ATP synthesis by calcium: Evidence for a long-term metabolic priming
Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A., & Rizzuto, R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.24.13807 · Cited by 814 · see citing works
Mallilankaraman, K. B., Doonan, P. J., Cárdenas, C., Chandramoorthy, H. C. K., Müller, M., Miller, R., Hoffman, N. E., Gandhirajan, R. K., Molgó, J., Birnbaum, M. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.10.011 · Cited by 661 · see citing works
Role of Mitochondrial Ca2+ in the Regulation of Cellular Energetics
Glancy, B. C., & Balaban, R. S. (2012) · Biochemistry · doi:10.1021/bi2018909 · Cited by 649 · see citing works
Ca2+ Indicators Based on Computationally Redesigned Calmodulin-Peptide Pairs
Palmer, A. E., Giacomello, M., Kortemme, T., Hires, S. A., Lev‐Ram, V., Baker, D. A., & Tsien, R. Y. (2006) · Chemistry & Biology · doi:10.1016/j.chembiol.2006.03.007 · Cited by 510 · see citing works
Measuring calcium signaling using genetically targetable fluorescent indicators
Palmer, A. E., & Tsien, R. Y. (2006) · Nature Protocols · doi:10.1038/nprot.2006.172 · Cited by 463 · see citing works
Barth, E. (1992) · Journal of Molecular and Cellular Cardiology · doi:10.1016/0022-2828(92)93381-s · Cited by 439 · see citing works
Mitochondria: The Hub of Cellular Ca2+Signaling
Szabadkai, G., & Duchen, M. R. (2008) · Physiology · doi:10.1152/physiol.00046.2007 · Cited by 403 · see citing works
Maack, C., Cortassa, S. C., Aon, M. A., Ganesan, A. N., Liu, T., & O'Rourke, B. P. (2006) · Circulation Research · doi:10.1161/01.res.0000232546.92777.05 · Cited by 369 · see citing works
Williams, G. S. B., Boyman, L., Chikando, A. C., Khairallah, R. J., & Lederer, W. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300410110 · Cited by 362 · see citing works
The mitochondrial permeability transition pore: a mystery solved?
Bernardi, P. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00095 · Cited by 335 · see citing works
The Ins and Outs of Mitochondrial Calcium
Finkel, T., Menazza, S., Holmström, K. M., Parks, R. J., Liu, J. C., Sun, J., Liu, J., Pan, X., & Murphy, E. (2015) · Circulation Research · doi:10.1161/circresaha.116.305484 · Cited by 289 · see citing works
Excitation-contraction coupling and mitochondrial energetics
Maack, C., & O'Rourke, B. P. (2007) · Basic Research in Cardiology · doi:10.1007/s00395-007-0666-z · Cited by 254 · see citing works
Ca2+ transport by mammalian mitochondria and its role in hormone action
Denton, R. M., & McCormack, J. G. (1985) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1985.249.6.e543 · Cited by 244 · see citing works
Liu, T., & O'Rourke, B. P. (2008) · Circulation Research · doi:10.1161/circresaha.108.175919 · Cited by 226 · see citing works
Mitochondrial Ca 2+ uptake contributes to buffering cytoplasmic Ca 2+ peaks in cardiomyocytes
Drago, I., Stefani, D. D., Rizzuto, R., & Pozzan, T. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210718109 · Cited by 218 · see citing works
Calcium Signal Transmission between Ryanodine Receptors and Mitochondria
Szalai, G., Csordás, G., Hantash, B. M., Thomas, A. P., & Hajnóczky, G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.20.15305 · Cited by 218 · see citing works
Cortassa, S. C., Aon, M. A., O'Rourke, B. P., Jacques, R., Tseng, H.-J., Marbán, E., & Winslow, R. L. (2006) · Biophysical Journal · doi:10.1529/biophysj.105.076174 · Cited by 208 · see citing works
Selectivity of Inhibition of Na+-Ca2+ Exchange of Heart Mitochondria by Benzothiazepine CGP-37157
Cox, D. A., Conforti, L., Sperelakis, N., & Matlib, M. A. (1993) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199304000-00013 · Cited by 184 · see citing works
NCLX: The mitochondrial sodium calcium exchanger
Boyman, L., Williams, G. S. B., Khananshvili, D., Sekler, I., & Lederer, W. J. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.03.012 · Cited by 172 · see citing works
SR and mitochondria: Calcium cross-talk between kissing cousins
Dorn, G. W., & Maack, C. (2012) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2012.07.015 · Cited by 141 · see citing works
Lu, X., Ginsburg, K. S., Kettlewell, S., Bossuyt, J., Smith, G. L., & Bers, D. M. (2012) · Circulation Research · doi:10.1161/circresaha.111.300501 · Cited by 130 · see citing works
Calcium release microdomains and mitochondria
Kohlhaas, M., & Maack, C. (2013) · Cardiovascular Research · doi:10.1093/cvr/cvt032 · Cited by 112 · see citing works
ER-Mitochondria Communication. How Privileged?
Franzini-Armstrong, C. (2007) · Physiology · doi:10.1152/physiol.00017.2007 · Cited by 109 · see citing works
Improved strategies for the delivery of GFP-based Ca2+ sensors into the mitochondrial matrix
Filippin, L., Cano‐Abad, M. F., Gastaldello, S., Magalhães, P. J., Sandonà, D., & Pozzan, T. (2004) · Cell Calcium · doi:10.1016/j.ceca.2004.08.002 · Cited by 109 · see citing works
Individual Cardiac Mitochondria Undergo Rare Transient Permeability Transition Pore Openings
Lu, X., Kwong, J. Q., Molkentin, J. D., & Bers, D. M. (2015) · Circulation Research · doi:10.1161/circresaha.115.308093 · Cited by 109 · see citing works
Mitochondrial Ca2+ uptake: Tortoise or hare?
O'Rourke, B. P., & Blatter, L. A. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2008.12.011 · Cited by 105 · see citing works
Dash, R. K., & Beard, D. A. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.151977 · Cited by 98 · see citing works
Andrienko, T., Picht, E., & Bers, D. M. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.03.015 · Cited by 88 · see citing works
Hüser, J., Blatter, L. A., & Sheu, S. (2000) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1005556227425 · Cited by 84 · see citing works
Olivetti, G., Quaini, F., Lagrasta, C. A. M., Ricci, R., Tiberti, G., Capasso, J. M., & Anversa, P. (1992) · PubMed Central · Cited by 81 · see citing works
Wei, A., Liu, T., Winslow, R. L., & O'Rourke, B. P. (2012) · The Journal of General Physiology · doi:10.1085/jgp.201210784 · Cited by 81 · see citing works
Calcium Movement in Cardiac Mitochondria
Boyman, L., Chikando, A. C., Williams, G. S. B., Khairallah, R. J., Kettlewell, S., Ward, C. W., Smith, G. L., Kao, J. P. Y., & Lederer, W. J. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2014.07.045 · Cited by 72 · see citing works
Kettlewell, S., Cabrero, P., Nicklin, S. A., Dow, J. A. T., Davies, S. A., & Smith, G. L. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.02.016 · Cited by 66 · see citing works
Integration of rapid cytosolic Ca2+ signals by mitochondria in cat ventricular myocytes
Sedova, M., Dedkova, E. N., & Blatter, L. A. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00619.2005 · Cited by 66 · see citing works
Control and Regulation of Mitochondrial Energetics in an Integrated Model of Cardiomyocyte Function
Cortassa, S. C., O'Rourke, B. P., Winslow, R. L., & Aon, M. A. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2008.12.3893 · Cited by 65 · see citing works
Genetically Encoded Ca 2+ Indicators in Cardiac Myocytes
Kaestner, L., Scholz, A., Tian, X. Y., Ruppenthal, S., Tabellion, W., Wiesen, K., Katus, H. A., Müller, O. J., Kotlikoff, M. I., & Lipp, P. (2014) · Circulation Research · doi:10.1161/circresaha.114.303475 · Cited by 63 · see citing works
Tian, X. Y., Pahlavan, S., Oleinikow, K., Jung, J., Ruppenthal, S., Scholz, A., Schumann, C., Kraegeloh, A., Oberhofer, M., Lipp, P., et al. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.09.001 · Cited by 57 · see citing works
Fowler, E. D., Benoîst, D., Drinkhill, M. J., Stones, R., Helmes, M., Wüst, R. C. I., Stienen, G. J. M., Steele, D. S., & White, E. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.06.016 · Cited by 49 · see citing works
Self-citationPapp, Z., Szabó, Á., Barends, J. P. F., & Stienen, G. J. M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.022145 · Cited by 46 · see citing works
Self-citationGriffiths, E. J. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1311 · Cited by 41 · see citing works
Isolation and Genetic Manipulation of Adult Cardiac Myocytes for Confocal Imaging
Kaestner, L., Scholz, A., Hammer, K. P., Vecerdea, A., Ruppenthal, S., & Lipp, P. (2009) · Journal of Visualized Experiments · doi:10.3791/1433 · Cited by 34 · see citing works
R-CEPIA1er as a new tool to directly measure sarcoplasmic reticulum [Ca] in ventricular myocytes
Bovo, E., Martin, J. W., Tyryfter, J., de Tombe, P. P., & Zima, A. V. (2016) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00175.2016 · Cited by 30 · see citing works
Self-citationRole of polyhydroxybutyrate in mitochondrial calcium uptake
Smithen, M., Elustondo, P. A., Winkfein, R. J., Zakharian, E., Abramov, A. Y., & Pavlov, E. V. (2013) · Cell Calcium · doi:10.1016/j.ceca.2013.04.006 · Cited by 29 · see citing works
Scorzeto, M., Giacomello, M., Toniolo, L., Canato, M., Blaauw, B., Paolini, C., Protasi, F., Reggiani, C., & Stienen, G. J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074919 · Cited by 27 · see citing works
Self-citationVentura, C., Ferroni, C., Flamigni, F., Stefanelli, C., & Capogrossi, M. C. (1994) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1994.267.2.h587 · Cited by 21 · see citing works
Haviland, S., Cleemann, L. N., Kettlewell, S., Smith, G. L., & Morad, M. (2014) · Cell Calcium · doi:10.1016/j.ceca.2014.06.001 · Cited by 17 · see citing works
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Bertero, E., & Maack, C. (2018) · Circulation Research · doi:10.1161/circresaha.118.310082 · Cited by 616 · see citing works
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Makrecka‐Kuka, M., Liepinsh, E., Murray, A. J., Lemieux, H., Dambrova, M., Tepp, K., Puurand, M., Käämbre, T., Han, W. H., de Goede, P., et al. (2019) · Acta Physiologica · doi:10.1111/apha.13430 · Cited by 93 · see citing works
Self-citationMiranda‐Silva, D., Wüst, R. C. I., Conceição, G., Gonçalves‐Rodrigues, P., Gonçalves, N., Gonçalves, A., Kuster, D. W. D., Leite-Moreira, A. F., van der Velden, J., Beleza, J., et al. (2019) · Acta Physiologica · doi:10.1111/apha.13378 · Cited by 77 · see citing works
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Self-citationAshok, D., Papanicolaou, K. N., Sidor, A., Wang, M. Y., Solhjoo, S., Liu, T., & O'Rourke, B. P. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104708 · Cited by 30 · see citing works
Marcucci, L., Canato, M., Protasi, F., Stienen, G. J. M., & Reggiani, C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201050 · Cited by 30 · see citing works
Self-citationWhy don't mice lacking the mitochondrial Ca2+ uniporter experience an energy crisis?
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Oropeza‐Almazán, Y., & Blatter, L. A. (2020) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00375.2020 · Cited by 27 · see citing works
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Ge, W.-D., Du, T.-T., Wang, C.-Y., Sun, L., & Wang, Y. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116278 · Cited by 18 · see citing works
Wang, H., Zhang, J., Hu, S. H., Tan, S. Z., Zhang, B., Zhou, H. M., & Peng, R. Y. (2018) · PubMed · doi:10.3967/bes2018.077 · Cited by 16 · see citing works
Solhjoo, S., Liu, T., Sidor, A., Lee, D. I., O'Rourke, B. P., & Steenbergen, C. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102780 · Cited by 13 · see citing works
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Liu, L., Zhou, K., Liu, X., Hua, Y., Wang, H., & Li, Y. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1013817 · Cited by 9 · see citing works
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Zhang, K., Lan, J., Leng, Y., & Xia, Z.-Y. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.108434 · Cited by 1 · see citing works
Luptak, I., Morgan, R. J., Baka, T., Croteau, D., Moverman, D. J., Sarnak, H., Kirber, M. T., Bachschmid, M. M., Colucci, W. S., & Pimentel, D. R. (2019) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2019.105569 · Cited by 1 · see citing works
Westerblad, H. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733699748.793549233
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Gökerküçük, E. B. (2022) · theses.fr (ABES) · doi:10.70675/5292e3e3z57efz4337z9710z536ed06cf7fb
- Authors
- Wüst, R. C. I., Helmes, M., Martin, J. L., van der Wardt, T. J. T., Musters, R. J. P., van der Velden, J., & Stienen, G. J. M.
- Affiliations
- Amsterdam Cardiovascular Sciences (NL)
- Cell and Molecular Physiology Loyola University Chicago IL USA
- Department of Physiology, Institute for Cardiovascular Research VU University Medical Centre Amsterdam the Netherlands
- Corresponding author
- Stienen, Ger J. M.
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2017-02-22
- Volume
- 595
- Issue
- 6
- Pages
- 2001-2019
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC5350475
- OpenAlex
- W2563463506
- Cited by
- 43
- References
- 49
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 6 · 2021: 3 · 2020: 6 · 2019: 6 · 2018: 8 · 2017: 1
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- VU Research Portal (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Hartstichting
- European Commission (FP7‐Health‐2010, 261409)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Keywords
- cardiomyocytes, stimulation frequency, mitochondrial calcium uptake, mitochondrial calcium release, mitochondrial calcium buffering, mitochondrial ATP production, energy supply and demand, intracellular calcium, electrical stimulation
- MeSH terms
- Adenosine Triphosphate, Animals, Calcium, Cytosol, Electric Stimulation, Mitochondria, Heart, Rats, Wistar, Sodium-Calcium Exchanger, Myocytes, Cardiac
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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