Skip to main content
SpringerLink
Log in

Physiological role of mitochondrial Ca2+ transport

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

A model has been proposed in which mitochondrial Ca2+ ion transport serves to regulate mitochondrial matrix free Ca2+ ([Ca2+]m), with the advantage to the animal that this allows the regulation of pyruvate dehydrogenase and the tricarboxylate cycle in response to energy demand. This article examines recent evidence for dehydrogenase activation and for increases in [Ca2+]m in response to increased tissue energy demands, especially in cardiac myocytes and in heart. It critiques recent results on beat-to-beat variation in [Ca2+]m in cardiac muscle and also briefly surveys the impact of mitochondrial Ca2− transport on transient changes in cytosolic free Ca2+ in excitable tissues. Finally, it proposes that a failure to elevate [Ca2+]m sufficiently in response to work load may underlie some cardiomyopathies of metabolic origin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Åkerman, K. E. O., and Nicholls, D. G. (1983).Rev. Physiol. Biochem. Pharmacol. 95 149–201.

    Google Scholar 

  • Allen, S. P., Stone, D., and McCormack, J. G. (1992).J. Mol. Cell. Cardiol. 24 765–774.

    Google Scholar 

  • Allen, S. P., Darley-Usmar, V. M. McCormack, J. G., and Stone, D. (1993).J. Mol. Cell. Cardiol. 25 949–958.

    Google Scholar 

  • Allshire, A., Piper, H. M., Cuthbertstone, K. S. R., and Cobbold, P. H. (1987).Biochem. J. 244 381–385.

    Google Scholar 

  • Al Nasser, I., and Crompton, M. (1986).Biochem. J. 239 19–29.

    Google Scholar 

  • Altschuld, R. A., Hohl, C. M., Castillo, L. C., Garleb, A. A., Starling, R. C., and Brierley, G. P. (1992).Am. J. Physiol. 262 H1699-H1704.

    Google Scholar 

  • Ashcroft, F. M., and Rorsman, P. (1990).Prog. Mol. Biol. Biophys. 54 87–143.

    Google Scholar 

  • Assimacopoulos-Jeannet, F., McCormack, J. G., and Jeanrenaud, B. (1986).J. Biol. Chem. 261 8799–8804.

    Google Scholar 

  • Baker, P. F., and Umbach, J. A. (1987).J. Physiol. 383 369–394.

    Google Scholar 

  • Balaban, R. S., Kantor, H. L., Katz, L. A., and Briggs, R. W. (1986).Science 232 1121–1123.

    Google Scholar 

  • Benzi, R. H., and Lerch, R. (1992).Circ. Res. 71 567–576.

    Google Scholar 

  • Berridge, M. J., and Galione, A. (1988).FASEB J. 2 3074–3082.

    Google Scholar 

  • Berridge, M. J., Cobbold, P. H., and Cuthbertson, K. S. R. (1988).Philos. Trans. R. Soc. London B 320 325–343.

    Google Scholar 

  • Blaustein, M. P., (1975).J. Physiol. (London) 247 617–655.

    Google Scholar 

  • Bond, M., Jaraki, A.-R., Disch, C. H., and Healy, B. P. (1989).Circ. Res. 64 1001–102.

    Google Scholar 

  • Bond, M., Vadasz, G., Somlyo, A. V., and Somlyo, A. P. (1987).J. Biol. Chem. 262 15630–15636.

    Google Scholar 

  • Broekemeier, K. M., Carpenter Deyo, L., Reed, D. J., and Pfeiffer, D. R. (1992).FEBS Lett. 304 192–194.

    Google Scholar 

  • Brown, G. C., Lakin-Thomas, P. L., and Brand, M. D. (1990).Eur. J. Biochem. 192 355–362.

    Google Scholar 

  • Chacon, E., Harper, I. S., Reece, J. M., Herman, B., and Lemasters, J. J. (1993).Biophys. J. 64, A106.

    Google Scholar 

  • Chapman, R. A. (1986).J. Physiol. 373 163–179.

    Google Scholar 

  • Chappell, J. B., Cohn, M., and Greville, G. D. (1963). InEnergy-Linked Functions of Mitochondria, Academic Press, New York, pp. 219–231.

    Google Scholar 

  • Chatham, J. C., and Forder, J. R. (1993).J. Mol. Cell. Cardiol. 25 1203–1213.

    Google Scholar 

  • Clarke, K., and Willis, R. J. (1987).J. Mol. Cell. Cardiol. 19 1153–1160.

    Google Scholar 

  • Coll, K. E., Joseph, S. K., Corkey, B. E., and Williamson, J. R. (1982).J. Biol. Chem. 257 8696–8704.

    Google Scholar 

  • Cox, D. A., and Matlib, M. A. (1993).J. Biol. Chem. 268 938–947.

    Google Scholar 

  • Crompton, M. (1985)Curr. Top. Membr. Transp. 25 231–276.

    Google Scholar 

  • Crompton, M., and Costi, A. (1990).Eur. J. Biochem. 178 489–501.

    Google Scholar 

  • Crompton, M., and Heid, I. (1978).Eur. J. Biochem. 91 599–608.

    Google Scholar 

  • Crompton, M., Sigel, E., Salzmann, M., and Carafoli, E. (1976a).Eur. J. Biochem. 69 429–434.

    Google Scholar 

  • Crompton, M., Capano, M., and Carafoli, E. (1976b).Eur. J. Biochem. 69 453–462.

    Google Scholar 

  • Crompton, M., Kessar, P., and Al-Nasser, I. (1983).Biochem. J. 216 333–342.

    Google Scholar 

  • Crompton, M., Ellinger, H., and Costi, A. (1988).Biochem. J. 255 357–360.

    Google Scholar 

  • Das, A. M., and Harris, D. A. (1990a).Am. J. Physiol. 259 H1264-H1269.

    Google Scholar 

  • Das, A. M., and Harris, D. A. (1990b).Cardiovasc. Res. 24 411–417.

    Google Scholar 

  • Davis, M. H., Altschuld, R. A., Jung, D. W., and Brierley, G. P. (1987).Biochem. Biophys. Res. Commun. 149 40–45.

    Google Scholar 

  • Denton, R. M., and McCormack, J. G. (1980).FEBS Lett. 119 1–8.

    Google Scholar 

  • Denton, R. M., and McCormack, J. G. (1985).Am. J. Physiol. 249 (Endocrinol. Metab. 12), E543-E554.

    Google Scholar 

  • Denton, R. M., Randle, P. J., and Martin, B. R. (1972).Biochem. J. 128 161–163.

    Google Scholar 

  • Denton, R. M., Richards, D. A., and Chen, J. G. (1978).Biochem. J. 176 899–906.

    Google Scholar 

  • Denton, R. M., McCormack, J. G., and Edgell, N. J. (1980).Biochem. J. 190 107–117.

    Google Scholar 

  • Dhalla, H. S., Sulakhe, P. V., Fedelson, M., and Yates, J. C. (1974).Adv. Cardiol. 13 282–300.

    Google Scholar 

  • Di Lisa, F., Fan, C.-Z., Gambassi, G., Hogue, B. A., Kudryashova, I., and Hansford, R. G. (1993a).Am. J. Physiol. 264 H2188–2197.

    Google Scholar 

  • Di Lisa, F., Gambassi, G., Spurgeon, H., and Hansford, R. G. (1993b).Cardiovasc. Res. 27 1840–1844.

    Google Scholar 

  • Duchen, M. R. (1992).Biochem. J. 283 41–50.

    Google Scholar 

  • Duchen, M. R., Valdeolmillos, M., O'Neill, S. C., and Eisner, D. A. (1990).J. Physiol. 424 411–426.

    Google Scholar 

  • Duchen, M. R., Smith. P. A., and Ashcroft, F. M. (1993).Biochem. J. 294 35–42.

    Google Scholar 

  • From, A. H. L., Petein, M. A., Michurski, S. P., Zimmer, S. D., and Ugurbil, K. (1986).FEBS Lett. 206 257–261.

    Google Scholar 

  • Fry, C. H., Powell, T., Twist, V. W., and Ward, J. P. T. (1984).Proc. R. Soc. London B 223 239–254.

    Google Scholar 

  • Griese, M., Perlitz, V., Jüngling, E., and Kammermeier, H. (1988).J. Mol. Cell. Cardiol. 20,

  • Gunter, T. E., and Pfeiffer, D. R. (1990).Am. J. Physiol. 258 (Cell Physiol. 27), C755-C786.

    Google Scholar 

  • Gunter, T. E., Restrepo, D., and Gunter, K. K. (1988).Am. J. Physiol. 255 C304-C310.

    Google Scholar 

  • Gupta, M. P., Innes, I. R., and Dhalla, N. S. (1988).Am. J. Physiol. 255 H1413-H1420.

    Google Scholar 

  • Gupta, M. P., Dixon, I. M. C., Zhao, D., and Dhalla, N. S. (1989).Can. J. Cardiol. 5 55–63.

    Google Scholar 

  • Hak, J. B., Van Beek, J. H. G. M., Eijgelshoven, M. H. J., and Westerhof, N. (1993).Am. J. Physiol. 264 (Heart Circ. Physiol. 33), H448-H453.

    Google Scholar 

  • Hansford, R. G. (1976).J. Biol. Chem. 251 5483–5489.

    Google Scholar 

  • Hansford, R. G. (1985).Rev. Physiol. Biochem. Pharmacol. 102 1–72.

    Google Scholar 

  • Hansford, R. G. (1987).Biochem. J. 241 145–151.

    Google Scholar 

  • Hansford, R. G. (1991).J. Bioenerg. Biomembr. 23 823–854.

    Google Scholar 

  • Hansford, R. G., and Castro, F. (1981).Biochem. J. 198 525–533.

    Google Scholar 

  • Hansford, R. G., and Castro, F. (1982).J. Bioenerg. Biomembr. 14 361–376.

    Google Scholar 

  • Hansford, R. G., and Castro, F. (1985).Biochem. J. 227 129–136.

    Google Scholar 

  • Hansford, R. G., Hogue, B., Prokopczuk, A., Wasilewska-Dziubińska, E., and Lewartowski, B. (1990).Biochim. Biophys. Acta 1018 282–286.

    Google Scholar 

  • Harris, D. A., and Das, A. M. (1991).Biochem. J. 280 561–573.

    Google Scholar 

  • Heineman, F. W., and Balaban, R. S. (1990).Annu. Rev. Physiol. 52 523–542.

    Google Scholar 

  • Heinrich, R., and Rapoport, T. A. (1974).Eur. J. Biochem. 42 89–95.

    Google Scholar 

  • Herman, B., Gores, G. J., Nieminen, A. L., Kawanishi, T., Harman, A., and Lemasters, J. J. (1990).Crit. Rev. Toxicol. 21 127–148.

    Google Scholar 

  • Hunter, D. R., Komai, H., Haworth, R. A., Jackson, M. D., and Berkoff, H. A. (1980).Circ. Res. 47 721–727.

    Google Scholar 

  • Isenberg, G., Han, S., Schiefer, A., and Wendt-Gallitelli, M.-F. (1993).Cardiovasc. Res. 27 1800–1809.

    Google Scholar 

  • Jou, M.-J., and Sheu, S.-S. (1994).Biophys. J. 66, A94.

  • Kacser, H., and Burns, J. A. (1973).Symp. Soc. Exp. Biol. 27 65–104.

    Google Scholar 

  • Kacser, H., and Porteous, J. W. (1987).Trends Biochem. Sci. 12 5–14.

    Google Scholar 

  • Kammermeier, H., Schmidt, P., and Jungling, E. (1982).J. Mol. Cell. Cardiol. 14 267–277.

    Google Scholar 

  • Katz, A. M. (1991).Hosp. Pract., Aug. 15, 78–90.

    Google Scholar 

  • Katz, B., and Miledi, R. (1967).Proc. R. Soc. London Ser. B. 167 23–38.

    Google Scholar 

  • Katz, L. A., Koretsky, A. P., and Balaban, R. S. (1987).FEBS Lett. 221 270–276.

    Google Scholar 

  • Katz, L. A., Koretsky, A. P., and Balaban, R. S. (1988).Am. J. Physiol. 255 (Heart Circ. Physiol 24), H185-H188.

    Google Scholar 

  • Katz, L. A., Swain, J. A., Portman, M. A., and Balaban, R. S. (1989).Am. J. Physiol. 256 (Heart Circ. Physiol. 25), H265-H274.

    Google Scholar 

  • Kawanishi, T., Blank, L. M., Harootunion, A. T., Smith, M. T., and Tsien, R. Y. (1989).J. Biol. Chem. 264 12859–12866.

    Google Scholar 

  • Leisey, J. R., Grotyohann, L. W., Scott, D. A., and Scaduto, R. C., Jr. (1993).Am. J. Physiol. 265 H1203-H1208.

    Google Scholar 

  • Lenzen, S., Hickethier, R., and Panten, U. (1986).J. Biol. Chem. 261 16478–16483.

    Google Scholar 

  • Li, Q., Altschuld, R. A., and Stokes, B. T. (1988).Am. J. Physiol. 255 C162-C168.

    Google Scholar 

  • Loew, L. M., Tuft, R. A., Carrington, W., and Fay, F. S. (1993).Biophys. J. 65 2396–2407.

    Google Scholar 

  • Longo, E. A., Tornheim, K., Deeney, J. T., Varnum, B. A., Tillotson, D., Prentki, M., and Corkey, B. E. (1991).J. Biol. Chem. 266 9314–9319.

    Google Scholar 

  • Lukács, G. L., and Kapus, A. (1987).Biochem. J. 248 609–613.

    Google Scholar 

  • Lukács, G. L., Kapus, A., and Fonyo, A. (1988) FEBS Lett.229 219–223.

    Google Scholar 

  • Markiewicz, W., Wu, S. S., Parmley, W. W., Higgins, C. B., Sievers, R., James, T. L. Wikman-Coffelt, J., and James, G. (1986).Circ. Res. 59 597–604.

    Google Scholar 

  • Martínez-Serrano, A., and Satrústegui, J. (1992).Mol. Biol. Cell 3 235–248.

    Google Scholar 

  • McCord, J. M. (1987).Fed. Proc. 46 2402–2406.

    Google Scholar 

  • McCormack, J. G., and Denton, R. M. (1979).Biochem. J. 180 533–544.

    Google Scholar 

  • McCormack, J. G., and Denton, R. M. (1981).Biochem. J. 196 619–624.

    Google Scholar 

  • McCormack, J. G., and Denton, R. M. (1984).Biochem. J. 218 235–247.

    Google Scholar 

  • McCormack, J. G., and England, P. J. (1983).Biochem. J. 214 581–585.

    Google Scholar 

  • McCormack, J. G., Browne, H. M., and Dawes, N. J. (1989).Biochim. Biophys. Acta 973 420–427.

    Google Scholar 

  • McCormack, J. G., Halestrap, A. P., and Denton, R. M. (1990a).Physiol. Rev. 70 391–425.

    Google Scholar 

  • McCormack, J. G., Longo, E. A., and Corkey, B. E. (1990b).Biochem. J. 267 527–530.

    Google Scholar 

  • Miyata, H., Silverman, H. S., Sollott, S. J., Lakatta, E. G., Stern, M. D., and Hansford, R. G. (1991). Am. J. Physiol.261 (Heart Circ. Physiol. 30), H1123-H1134.

    Google Scholar 

  • Miyata, H., Lakatta, E. G., Stern, M. D., and Silverman, H. S. (1992).Circ. Res. 71 605–613.

    Google Scholar 

  • Moravec, C. S., and Bond, M. (1991).Am. J. Physiol. 260 H989-H997.

    Google Scholar 

  • Moravec, C. S., and Bond, M. (1992).J. Biol. Chem. 267 5310–5316.

    Google Scholar 

  • Moravec, C. S., Desnoyer, R. W., Milovanovic, M., and Bond, M. (1994).Biophys. J. 66, A92.

    Google Scholar 

  • Moreno-Sánchez, R., and Hansford, R. G. (1988).Biochem. J. 256 403–412.

    Google Scholar 

  • Nazareth, W., Yafei, N., and Crompton, M. (1991).J. Mol. Cell. Cardiol. 23 1351–1354.

    Google Scholar 

  • Nicholls, D. G. (1978).Biochem. J. 176 463–474.

    Google Scholar 

  • Proschek, L., and Jasmin, G. (1982).Muscle Nerve 5 26–32.

    Google Scholar 

  • Raiteri, M., and Levi, G. (1978).Rev. Neurosci. 3 77–111.

    Google Scholar 

  • Reed, K. C., and Bygrave, F. L. (1974).Biochem. J. 140 143–155.

    Google Scholar 

  • Reed, L. J., Damuni, Z., and Merryfield, M. L. (1985).Curr. Top. Cell. Regul. 27 41–49.

    Google Scholar 

  • Reers, M., Kelly, R. A., and Smith, T. W. (1989).Biochem. J. 257 131–142.

    Google Scholar 

  • Rink, T. J., and Hallam, T. J. (1989).Cell. Calcium 10 385–395.

    Google Scholar 

  • Rizzuto, R., Simpson, A. W. M., Brini, M., and Pozzan, T. (1992).Nature (London) 358 325–327.

    Google Scholar 

  • Rizzuto, R., Brini, M., Murgia, M., and Pozzan, T. (1993).Science 262 744–747.

    Google Scholar 

  • Robertson, S. P., Potter, J. P., and Rouslin, W. (1982).J. Biol. Chem. 257 1743–1748.

    Google Scholar 

  • Rodrigues, B., and McNeill, J. H. (1992).Cardiovasc. Res. 26 913–922.

    Google Scholar 

  • Rossi, C. S., Vasington, F. D., and Carafoli, E. (1973).Biochem. Biophys. Res. Commun. 50 846–852.

    Google Scholar 

  • Rutter, G. A., Theler, J.-M., Murgia, M., Wollheim, C. B., Pozzan, T., and Rizzuto, R. (1993).J. Biol. Chem. 268 22385–22390.

    Google Scholar 

  • Schaffer, W. T., and Olson, M. S. (1980).Biochem. J. 192 741–751.

    Google Scholar 

  • Sollott, S. J., and Lakatta, E. G. (1994).Am. J. Physiol., in press.

  • Sollott, S. J., Ziman, B. D., and Lakatta, E. G. (1992).Am. J. Physiol. 262 H1941-H1949.

    Google Scholar 

  • Somlyo, A. P., Bond, M., and Somlyo, A. V. (1985).Nature (London) 314 622–625.

    Google Scholar 

  • Stern, M. D., Silverman, H. S., Houser, S. R., Josephson, R. A., Capogrossi, M. C., Nichols, C. G., Lederer, W. J., and Lakatta, E. G. (1988).Proc. Natl. Acad. Sci. USA 85 6954–6958.

    Google Scholar 

  • Stone, D., Darley-Usmar, V., Smith, D. R., and O'Leary, V. (1989).J. Mol. Cell. Cardiol.,21 963–973.

    Google Scholar 

  • Szabo, I., and Zoratti, M. (1991).J. Biol. Chem. 266 3376–3379.

    Google Scholar 

  • Thayer, S. A., and Miller, R. J. (1990).J. Physiol. 425 85–115.

    Google Scholar 

  • Unitt, J. F., McCormack, J. G., Reid, D., Maclachlan, L. K., and England, P. J. (1989).Biochem. J. 262 293–301.

    Google Scholar 

  • Wan, B., La Noue, K. F., Cheung, J. Y., and Scaduto, R. C., Jr. (1989).J. Biol. Chem. 264 13430–13439.

    Google Scholar 

  • Wendt-Gallitelli, M.-F., and Isenberg, G. (1991).J. Physiol. (London) 435 349–372.

    Google Scholar 

  • Wieland, O. H. (1983).Rev. Physiol. Biochem. Pharmacol. 96 123–170.

    Google Scholar 

  • Wikman-Coffelt, J., Sievers, R., Parmley, W. W., and Jasmin, G. (1986).Cardiovas. Res. 20 471–481.

    Google Scholar 

  • Wikman-Coffelt, J., Stefenelli, T., Wu, S. T., Parmley, W. W., and Jasmin, G. (1991).Circ. Res. 68 45–51.

    Google Scholar 

  • Wolska, B. M., and Lewartowski, B. (1991).J. Mol. Cell Cardiol. 23 217–226.

    Google Scholar 

  • Woods, N. M., Cuthbertson, K. S. R., and Cobbold, P. H. (1986).Nature (London) 319 600–602.

    Google Scholar 

  • Wrogemann, K., and Nylen, E. G. (1978).J. Mol. Cell. Cardiol. 10 185–195.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Gerontology Research Center, National Institute on Aging, 21224, Baltimore, Maryland

    Richard G. Hansford

Authors
  1. Richard G. Hansford
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hansford, R.G. Physiological role of mitochondrial Ca2+ transport. J Bioenerg Biomembr 26, 495–508 (1994). https://doi.org/10.1007/BF00762734

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00762734

Key words

Search

Navigation