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Modulation of cell calcium signals by mitochondria

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Abstract

It is now clearer and clearer that mitochondria play a role, and perhaps an active role, in cell calcium signalling. The fact that mitochondria can exhibit a Ca2+>-induced Ca2+> release (mCICR, Ichas et al. [37]) reinforces this concept and makes the mitochondria an essential element in the relay of Ca2+> wave propagation. It must be emphasized that the modulation of cell Ca2+> signals by mitochondria depends upon their energetic status, thus making mitochondria an essential link between energy metabolism and calcium signalling inside the cell.

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References

  1. Rizzuto R, Simpson AWM, Brini M, Pozzan T: Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358: 325–327, 1992

    Google Scholar 

  2. Rizzuto R, Brini M, Murgia M, Pozzan T: Microdomains with high Ca2+ close to IP3-sensitive channels are sensed by neighboring mitochondria. Science 262: 744–747, 1993

    Google Scholar 

  3. Rizzuto R, Bastianutto M, Brini M, Murgia M, Pozzan T: Mitochondrial Ca2+ homeostasis in intact cells. J Cell Biol 126: 1183–1194, 1994

    Google Scholar 

  4. Rutter GA, Theler JM, Murgia M, Wolheim CB, Pozzan T, Rizzuto R: Increased Ca2+ influx raises mitochondrial free Ca2+ to micromolar levers in a pancratic beta-cell line. J Biol Chem 268: 22385–22390, 1993

    Google Scholar 

  5. Lawrie AM, Rizzuto R, Pozzan T, Simpson AWM: A role for calcium influx in the regulation of mitochondrial calcium in endothelial cells. J Biol Chem 271: 10753–10759, 1996

    Google Scholar 

  6. Gunter TE, Gunter KK, Sheu SS, Gavin CE: Mitochondrial Ca2+ transport: Physiological and pathological relevance. Am J Physiol 267: C313–C339, 1994

    Google Scholar 

  7. McCormack JC, Halestrap AP, Denton RM: Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70: 391–495, 1990

    Google Scholar 

  8. McCormack JG, Denton RM: Signal transduction by intramitochondrial Ca2+ in mammalian energy metabolism. News Physiol Sci 9: 71–76, 1994

    Google Scholar 

  9. Gunter TE, Pfeiffer DR: Mechanisms by which mitochondria transport calcium. Am J Physiol 258: C755–C786, 1990

    Google Scholar 

  10. McMillin-Wood J, Wolkowicz PE, Chu A, Tate CA, Goldstone MA, Entman ML: Calcium uptake by two preparations of mitochondria from heart. Biochem Biophys Acta 591: 251–265, 1980

    Google Scholar 

  11. Bragadin M, Pozzan T, Azzone GF: Kinetics of Ca2+ carrier in rat liver mitochondria. Biochemistry 18: 5972–5978, 1979

    Google Scholar 

  12. Bygrave FL, Reed KC, Spencer T: Cooperative interactions in energydependent accumulation of Ca2+ by isolated rat liver mitochondria. Nature New Biol 230: 89–91, 1971

    Google Scholar 

  13. Heaton GM, Nicholls DG: The Ca2+ conductance of the inner membrane of rat liver mitochondria and the determination of the Ca2+ electrochemical gradient. Biochem J 156: 635–646, 1976

    Google Scholar 

  14. Huston SM, Pfeiffer DR, Lardy HA: Effect of cations and anions on the steady state kinetics of energy-dependent Ca2+ transport in rat liver mitochondria. J Biol Chem 251: 5251–5258, 1976

    Google Scholar 

  15. Reed KC, Bygrave FL: A kinetic study of mitochondrial Ca2+ transport. Eur J Biochem 55: 97–504, 1975

    Google Scholar 

  16. Vinogradov A, Scarpa A: The initial velocities of Ca2+ uptake by rat liver mitochondria. J Biol Chem 248: 5527–5531, 1975

    Google Scholar 

  17. Sparagna GC, Gunter KK, Sheu SS, Gunter TE: Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem 270: 27510–27515, 1995

    Google Scholar 

  18. Fiskum G, Lehninger AL: Regulated release of Ca2+/2H+ antiport. J Biol Chem 254: 6236–6239, 1979

    Google Scholar 

  19. Puskin JS, Gunter TE, Gunter KK, Russel PR: Evidence for more than one Ca2+ transport mechanism in mitochondria. Biochemistry 15: 3834–3842, 1976

    Google Scholar 

  20. Crompton M, Capano M, Carafoli E: The sodium-induced efflux of calcium from heart mitochondria. A possible mechanism for the regulation of mitochondrial transport. Eur J Biochem 69: 453–4562, 1976

    Google Scholar 

  21. Crompton M, Heid I: The cycling of Ca2+, Na2+, and H+ across the inner membrane of cardiac mitochondria. Eur J Biochem 91: 599–608, 1978

    Google Scholar 

  22. Crompton M, Kunzi M, Carafoli E: The calcium-induced and sodium-induced effluxes of calcium from heart mitochondria. Eur J Biochem 79: 549–558, 1977

    Google Scholar 

  23. Wingrove DE, Gunter TE: Kinetics of mitochondrial calcium transport. II. A kinetic description of the sodium-dependent calcium efflux mechanism of liver mitochondria and inhibition by ruthenium red and by tetraphenylphosphonium. J Biol Chem 261: 15166–15171, 1986

    Google Scholar 

  24. Gavin CE, Gunter KK, Gunter TE: Mn2+ transport across biological membranes may be monitored spectroscopically using Ca2+ indicator dye antipyrylazo III. Anal Biochem 192: 44–48, 1991

    Google Scholar 

  25. Zoratti M, Szabò I: The mitochondrial permeability transition. Biochem Biophys Acta 1241: 139–176, 1995

    Google Scholar 

  26. Petronilli V, Szabò I, Zoratti M: The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria. FEBS Lett 259: 137–143, 1989

    Google Scholar 

  27. Tedeschi H, Kinnaly KW, Mannella CA: Properties of channels in the mitochondrial outer membrane. J Bioenerg Biomembr 21: 451–559, 1989

    Google Scholar 

  28. Kinnaly KW, Zorov D, Antonenko Y, Perini S: Calcium modulation of the mitochondrial inner membrane channel activity. Biochem Biophys Res Commun 176: 1183–1188, 1991

    Google Scholar 

  29. Szabò I, Zoratti M: The giant channel of the inner mitochondrial membrane is inhibited by cyclosporine A. J Biol Chem 267: 3376–3379, 1991

    Google Scholar 

  30. Szabò I, Zoratti M: The mitochondrial megachannel is the permeability transition pore. J Bioenerg Biomembr 24: 111–117, 1992

    Google Scholar 

  31. Bernardi P, Broekemeir KM, Pfeiffer DR: Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26: 509–517, 1994

    Google Scholar 

  32. Petronilli V, Cola C, Bernardi P: Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore. J Biol Chem 268: 1011–1016, 1993

    Google Scholar 

  33. Nicolli A, Petronilli V, Bernardi P: Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by matrix pH. Evidence that the pore open-closed probability is regulated by reversible histidine protonation. Biochem 32: 4461–4465, 1993

    Google Scholar 

  34. Altschuld RA, Hohl CM, Castillo LC, Garleb AA, Starling RC, Brierley GP: Cyclosporin inhibits mitochondrial calcium efflux in isolated adult rat ventricular cardiomyocytes. Am J Physiol 262: H1699–H1704, 1992

    Google Scholar 

  35. Meissner G: Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem 261: 6300–6306, 1986

    Google Scholar 

  36. Bernardi P, Petronilli V: The permeability transition pore as a mitochondrial calcium release channel; a critical appraisal. J Bioenerg Biomembr 28: 129–136, 1996

    Google Scholar 

  37. Ichas F, Jouaville LS, Sidash SS, Mazat J-P, Holmuhamedov EL: Mitochondrial calcium spiking: A transduction mechanism based on calcium-induced permeability transition involved in cell calcium signaling. FEBS Lett 348: 211–215, 1994

    Google Scholar 

  38. Friel DD, Tsien RW: An FCCP-sensitive Ca2+ store in bullfrog sympathetic neurons and its participation in stimulus-evoked changes in [Ca2+]i. J Neurosci 14: 4007–4024, 1994

    Google Scholar 

  39. Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD: Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 77: 438–441, 1996

    Google Scholar 

  40. Herrington J, Park YB, Babcock DF, Hille B: Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells. Neuron 16: 219–228, 1996

    Google Scholar 

  41. Budd SL, Nicholls DG: A re-evaluation of the role of mitochondria in neuronal calcium homeostasis. J Neurochem 66: 403–411, 1996

    Google Scholar 

  42. Babcock DF, Herrington J, Goodwin PC, Park YB, Hille B: Mitochondrial participation in the intracellular Ca2+ network. J Cell Biol 136: 833–844, 1997

    Google Scholar 

  43. Simpson PB, Russel JT: Mitochondria support inositol 1,4,5-trisphosphate-mediated Ca2+ waves in cultured oligodendrocytes. J Biol Chem 271: 33493–33501, 1996

    Google Scholar 

  44. Ichas F, Jouaville LS, Mazat JP: Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89: 1145–1153, 1997

    Google Scholar 

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Authors and Affiliations

  1. Laboratoire GESBI, Université Victor Ségalen, Bordeaux 2, 146 rue Léo Saignat, F-33076, Bordeaux-Cédex, France

    Laurence S. Jouaville, François Ichas & Jean-Pierre Mazat

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  1. Laurence S. Jouaville
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  2. François Ichas
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  3. Jean-Pierre Mazat
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Jouaville, L.S., Ichas, F. & Mazat, JP. Modulation of cell calcium signals by mitochondria. Mol Cell Biochem 184, 371–376 (1998). https://doi.org/10.1023/A:1006850121769

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