Role of calcium ions in regulation of mammalian intramitochondrial metabolism
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Matrix Ca2+ stimulates matrix dehydrogenases including pyruvate dehydrogenase and the TCA dehydrogenases.
“One candidate is the known effect of matrix Ca2+ in stimulating the matrix dehydrogenases including pyruvate dehydrogenase and the TCA dehydrogenases (McCormack et al., 1990).”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as McCormack et al., 1990
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“With low intensity stress, limited MPT leads to mitoptosis, which is followed by the elimination of degraded mitochondria.”
BackgroundInfluentialThe mitochondrial calcium uniporter is a highly selective ion channel
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“Several TCA-cycle enzymes, including pyruvate dehydrogenase and a-ketoglutarate dehydrogenase, are regulated by calcium (McCor- mack et al., 1990).”
InfluentialMitochondria and calcium: from cell signalling to cell death
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“…major targets of the mitochondrial Ca¥ import pathway are the dehydrogenases of the TCA cycle, as the ratelimiting enzymes are all upregulated by Ca¥-dependent processes, as discussed by Maechler & Wollheim (2000) and Rizzuto et al. (2000) (this issue, and see McCormack et al. 1990 for review).”
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“78 Increased mitochondrial Ca 2 + is bene fi cial up to a point; however, chronic mitochondrial Ca 2 + overload triggered Bcl-2-mediated regulated cell death, which is primarily mediated through the induction of the mitochondrial permeability transition pore (mPTP).”
BackgroundDecoding of cytosolic calcium oscillations in the mitochondria
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“We speculated that constitutive low-level InsP3R Ca 2+ release promotes oxidative phosphorylation by activation of the ATP synthase (Balaban, 2009; Territo et al., 2000) and/or dehydrogenases to provide reducing equivalents (McCormack et al., 1990).”
InfluentialRapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin
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“Sustained Ca can stimulate mitochondrial dehydrogenases, impairing the cell’s ability to suppress electron flux through the electron transport chain during hypoxia (McCormack et al. 1990).”
BackgroundRegulation of mitochondrial dehydrogenases by calcium ions
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“Early approaches before 1990 are reviewed in [6].”
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“Repetitive electrical stimulation of motor neurons (10–60 s, 50–100 Hz) resulted in an plateau elevation of [Ca(2) ]m in mitochondria in axon terminals to about 1 M (45), which is in the appropriate range for activation of mitochondrial dehydrogenases (145), but well below the value necessary for opening of the MPTP (…”
BackgroundInfluentialDistinct fission signatures predict mitochondrial degradation or biogenesis.
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“activity mediated by cyclic AMP and intramitochondrial [Ca(2) ] accumulation (38, 112, 113).”
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“An increase in [Ca(2) ]M can also activate several TCA cycle enzymes, leading to increased NADH production, secondary enhancement of electron transport, and repolarization of M (440, 1224).”
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“In the early 1990s it became clear that the three major rate limiting enzymes of the citric acid cycle are all upregulated by Ca2þ (McCormack et al., 1990).”
BackgroundThe permeability transition pore complex: another view
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“The resulting increase in matrix NADH/NAD stimulates respiration leading to an increase in proton motive force (pmf) and ATP production [14].”
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“Ca2+ flux across the inner mitochondrial membrane (IMM) regulates cell bioenergetics, cytoplasmic Ca2+ ([Ca]i) signals and activation of cell death pathways (Balaban, 2009; Denton and McCormack, 1980; Duchen et al., 2008; Gunter and Gunter, 1994; Hajnoczky et al., 1995; Hansford, 1994; Herrington et al., 1996; Lemaste…”
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“Intramitochondrial Ca(2) is recognized as an allosteric activator of matrix dehydrogenases, such as NAD -isocitrate dehydrogenase, pyruvate dehydrogenase and -ketoglutarate dehydrogenase (104) and as co-factor of mitochondrial nitric oxide (NO) synthase (mtNOS) (59).”
BackgroundRole 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
“With many cellular systems the addition of Ca2+, via a wide variety of methods, has convincingly demonstrated an activation of NAD(P)H generation by the entry of Ca2+ into the mitochondrial matrix (12).”
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“NADH and thus ATP production [55, 56].”
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“A substantial impetus was given to attempts to address these issues by the discovery that the key rate-limiting enzymes of the citric acid cycle are upregulated by Ca¥, either directly or through the regulation of phosphorylation reactions (for review, see McCormack et al. 1990).”
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“The rapid rise of Cam to even modest physiological Cac loads presumably also means that mitochondrial energy metabolism adjusts itself to cellular activities from moment to moment (McCormack et al., 1990; Gunter et al., 1994; Hajnóczky et al., 1995; Rutter et al., 1996).”
BackgroundEndoplasmic Reticulum and the Unfolded Protein Response
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“Additionally, also many other mitochondrial processes, such as fatty acid oxidation, amino acid catabolism, F1-ATPase manganese superoxide dismutase activity, aspartate and glutamate carrier, as well as the adenine-nucleotide translocase activity, are regulated by mitochondrial calcium (McCormack et al., 1990; Hayashi…”
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“Calcium is a well-known activator of mitochondrial dehydrogenases (for review see McCormack et al., 1990) and so Ca2 could be an ideal signal to synchronize cell function and mitochondrial metabolism during stimulation by Ca2 -mobilizing stimuli.”
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Mitochondrial function in normal and diabetic β-cells
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“At the same time, whereas pulsatile, transient increases in matrix [Ca] ([Ca]mt), which occur in stimulated cells, are essential for stimulating Casensitive dehydrogenases and upregulating ATP production (Jouaville et al., 1999; McCormack et al., 1990), continuous Ca accumulation in resting conditions would on the one…”
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Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons
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“Indeed, it has been suggested that intramitochondrial CaZ+ serves as a means to couple energy demands to ATP production (McCormack et al., 1990).”
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“…it became soon clear that the [Ca 2 þ ] mt changes modulate key cellular processes, such as aerobic metabolism (through Ca 2 þ -sensitive dehydrogenases; McCormack et al , 1990; Denton, 2009) and the release of pro-apoptotic factors (Szalai et al , 1999 Pinton et al , 2001; Scorrano et al , 2003).”
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“Key ETC proteins (subunits of ND and cytochrome b, for example) are encoded by the mitochondrial genome and since these proteins are translated in the mitochondrial matrix, coordinated induction of mitochondrial encoded tRNAs and rRNA expression is also required (104).”
BackgroundInfluentialMCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism
Mallilankaraman, K. B., Cárdenas, C., Doonan, P. J., Chandramoorthy, H. C. K., Irrinki, K. M., Golenár, T., Csordás, G., Madireddi, P., Yang, J., Müller, M., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2622 · Cited by 487 · see citing works
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“localized in the matrix, the pyruvate-, α-ketoglutarate- and isocitrate-dehydrogenases (collectively called the Ca2+-sensitive mitochondrial dehydrogenases, CSMDHs) are activated by Ca2+, with different mechanisms: the first through a Ca2+-dependent dephosphorylation step, the others via direct binding to a regulatory…”
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“Conversely, the sensitivity to staurosporinecreased cellular needs (McCormack et al., 1990).”
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“Moreover, when taken up by the mitochondria, Ca(2) can physiologically increase ATP generation by activating matrix dehydrogenases (6).”
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“Activation of the TCA cycle dehydrogenases by increasing mitochondrial calcium (McCormack et al., 1990) with the calcium ionophore A23187 (0.”
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“On one hand, an increase in [Ca 2 ] m can increase the production of ATP by activating matrix dehydrogenases in agonist-stimulated cells (McCormack et al., 1990; Robb-Gaspers et al., 1998; Jouaville et al., 1999).”
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“The activation of the PDC observed in working hearts submitted to increased workload or perfused with epinephrine appears to be the result of increased mitochondrial Ca 21 entry.(52)”
BackgroundEnjoy the Trip: Calcium in Mitochondria Back and Forth
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“The overall rate of the Krebs cycle is considered to be determined by the activities of citrate synthase, isocitrate dehydrogenase, and a-KGDH (Cooney et al., 1981; McCormack et al., 1990; Moreno-Sanchez et al., 1990).”
BackgroundHeart mitochondria: gates of life and death
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“For instance, uptake of Ca2þ results in the activation of three dehydrogenases in the mitochondrial matrix.(35) This causes an increase in mitochondrial NADH/NADþ ratio which may result in increased energy available for mitochondrial functions.”
BackgroundMallilankaraman, K. B., Cárdenas, C., Doonan, P. J., Chandramoorthy, H. C. K., Irrinki, K. M., Golenár, T., Csordás, G., Madireddi, P., Yang, J., Müller, M., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3202 · Cited by 418 · see citing works
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“ply of reducing equivalents [NAD(P)H+] (67, 84, 86).”
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“Mild increases in matrix Ca can stimulate activity of the tricarboxylic acid cycle enzymes pyruvate dehydrogenase, 2-oxoglutarate dehydrogenase and NAD-isocitrate dehydrogenase [127] leading to increased respiratory energy production.”
BackgroundEnergy metabolism of the heart: From basic concepts to clinical applications applications
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Mitochondrial dysfunction in neurodegenerative disorders
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“This ultimately increases ATP production [91,92].”
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“The increase in intermitochondrial Ca2+ is then able to escalate the rate of oxidative phosphorylation by activating isocitrate dehydrogenase, α-ketoglutarate dehydrogenase, and pyruvate dehydrogenase [44], which will also increase the amount of superoxide produced.”
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“In isolated mitochondria, Ca (21)stimulation can increase NADH (McCormack et al., 1990; Hansford and Zorov, 1998; Territo et al., 2000), but the magnitude of this increase will also depend on any downstream effects on NADH oxidation.”
BackgroundInfluentialMitochondrial calcium transport: mechanisms and functions
Gunter, T. E., Buntinas, L., Sparagna, G. C., Eliseev, R. A., & Gunter, K. K. (2000) · Cell Calcium · doi:10.1054/ceca.2000.0168 · Cited by 378 · see citing works
Mitochondrial calcium as a key regulator of mitochondrial ATP production in mammalian cells
Griffiths, E. J., & Rutter, G. A. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.01.019 · Cited by 379 · see citing works
“[10], and see chapter by Denton in this volume).”
BackgroundInfluentialEndothelial Mitochondria: Contributing to Vascular Function and Disease
Davidson, S. M., & Duchen, M. R. (2007) · Circulation Research · doi:10.1161/01.res.0000261970.18328.1d · Cited by 381 · see citing works
Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism
Yellen, G. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201803152 · Cited by 371 · see citing works
“, 2014) If both components of the NAD(P)H signal are substantially mitochondrial in origin, then what accounts for the overshoot? One candidate is the known effect of matrix Ca2+ in stimulating the matrix dehydrogenases including pyruvate dehydrogenase and the TCA dehydrogenases (McCormack et al., 1990).”
BackgroundIntegrating cytosolic calcium signals into mitochondrial metabolic responses
Gaspers, L. D., Burnett, P., Rutter, G. A., Denton, R. M., Rizzuto, R., & Thomas, A. P. (1998) · The EMBO Journal · doi:10.1093/emboj/17.17.4987 · Cited by 370 · see citing works
“…in the concentration of Ca2 in mitochondria ([Ca2 ]m), and that this is important for the stimulation of mitochondrial oxidative metabolism (McCormack et al., 1990; Duchen, © Oxford University Press 4987 1992; Loew et al., 1994; Rizzuto et al., 1994; Hajnóczky et al., 1995; Rutter et al.,…”
BackgroundSelf-citationLogan, C. V., Szabadkai, G., Sharpe, J. A., Parry, D. A., Torelli, S., Childs, A., Kriek, M., Phadke, R., Johnson, C. A., Roberts, N. Y., et al. (2013) · Nature Genetics · doi:10.1038/ng.2851 · Cited by 369 · see citing works
The role of the mitochondrial permeability transition pore in heart disease
Halestrap, A. P., & Pasdois, P. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.12.017 · Cited by 362 · see citing works
Self-citationTinel, H., Cancela, J., Mogami, H., Gerasimenko, J. V., Gerasimenko, O. V., Tepikin, A. V., & Petersen, O. H. (1999) · The EMBO Journal · doi:10.1093/emboj/18.18.4999 · Cited by 361 · see citing works
Mechanisms of Altered Ca 2+ Handling in Heart Failure
Luo, M., & Anderson, M. E. (2013) · Circulation Research · doi:10.1161/circresaha.113.301651 · Cited by 368 · see citing works
“reducing equivalents (NADH/NADPH) for electron transport.(116) Metabolic regulation by mitochondrial Ca uptake,”
A mitochondrial bioenergetic etiology of disease
Wallace, D. C. (2013) · Journal of Clinical Investigation · doi:10.1172/jci61398 · Cited by 342 · see citing works
Control of mitochondrial ATP synthesis in the heart
Harris, D. A., & Das, A. M. (1991) · Biochemical Journal · doi:10.1042/bj2800561 · Cited by 352 · see citing works
Cardiac Energy Metabolism Homeostasis: Role of Cytosolic Calcium
Balaban, R. S. (2002) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2002.2082 · Cited by 357 · see citing works
Plant organellar calcium signalling: an emerging field
Stael, S., Wurzinger, B., Mair, A., Mehlmer, N., Vothknecht, U. C., & Teige, M. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err394 · Cited by 344 · see citing works
“On the other hand, the elevation of Ca inside the mitochondria positively affects ATP production by up-regulating the major limiting enzymes of the citric acid cycle (similar to the up-regulation of the Calvin cycle in chloroplasts) (McCormack et al., 1990).”
BackgroundMitochondrial metabolism of reactive oxygen species
Venditti, P., Stefano, L. D., & Meo, S. D. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.01.008 · Cited by 346 · see citing works
“Conversely, under oxidative stress, mitochondrial Ca overload depresses mitochondrial function (McCormack et al., 1990) and primes different processes, which might lead to irreversible cell damage.”
BackgroundCa2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons
Duchen, M. R. (1992) · Biochemical Journal · doi:10.1042/bj2830041 · Cited by 338 · see citing works
Bound and determined: A computer program for making buffers of defined ion concentrations
Brooks, S. P. J., & Storey, K. B. (1992) · Analytical Biochemistry · doi:10.1016/0003-2697(92)90183-8 · Cited by 335 · see citing works
Manganese neurotoxicity and the role of reactive oxygen species
Martinez‐Finley, E. J., Gavin, C. E., Aschner, M., & Gunter, T. E. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.01.032 · Cited by 334 · see citing works
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“Volume-activation appears to play an important role in hormone-stimulated gluconeogenesis and FA oxidation, and stimulation of FA oxidation can be mimicked in hepatocytes by increasing matrix volume with low doses of valinomycin [167,168].”
BackgroundMitochondrial Ca2+ homeostasis in intact cells.
Rizzuto, R., Bastianutto, C., Brini, M., Murgia, M., & Pozzan, T. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.5.1183 · Cited by 322 · see citing works
Park, M. K., Ashby, M. C., Erdemli, G., Petersen, O. H., & Tepikin, A. V. (2001) · The EMBO Journal · doi:10.1093/emboj/20.8.1863 · Cited by 318 · see citing works
- Authors
- McCormack, J. G., Halestrap, A. P., & Denton, R. M.
- Affiliations
- University of Leeds (GB)
- ORCID
- Halestrap, A. P.
- Venue
- Physiological Reviews
- Publisher
- American Physiological Society
- Published
- 1990-04-01
- Volume
- 70
- Issue
- 2
- Pages
- 391-425
- ISSN
- 0031-9333 (ISSN-L)
- 1522-1210
- OpenAlex
- W1935060748
- Cited by
- 1,398
- References
- 0
- Citations by year
- 2026: 18 · 2025: 21 · 2024: 16 · 2023: 33 · 2022: 26 · 2021: 44 · 2020: 40 · 2019: 39 · 2018: 36 · 2017: 40 · 2016: 47 · 2015: 37 · 2014: 53 · 2013: 63 · 2012: 68
- FWCI
- 10.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiological Reviews (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
- Keywords
- calcium ions, mitochondrial calcium, calcium signaling, mammalian mitochondria
- MeSH terms
- Animals, Calcium, Humans, Ions, Mammals, Mitochondria, Osmolar Concentration, Oxidoreductases, Oxygen Consumption, Pyrophosphatases
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