Journal of Muscle Research & Cell Motility

, Volume 18, Issue 4, pp 473–483 | Cite as

Inhibition of mitochondrial calcium uptake slows down relaxation in mitochondria-rich skeletal muscles

  • J. M. GILLIS


Isolated fibres from various muscles were skinned mechanically in oil. From a Ca2+-loaded micropipette, local applications of Ca2+ were made. These produced a limited contraction which relaxed spontaneously. The time-course of sarcomere shortening and re-lengthening was recorded by microcinephotography. Application of Ruthenium Red, a potent and specific inhibitor of Ca2+ uptake by mitochondria, did not affect the contraction- relaxation cycles of typical glycolytic white fibres (frog sartorius, pigeon breast). By contrast, Ruthenium Red greatly slowed down the relaxation rate in mitochondria-rich fibres (rat soleus and rabbit masseter). In these fibres, Ca2+ uptake by mitochondria seems to play an active role in promoting relaxation


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  1. ASHLEY, C. C., CALDWELL, P. C., LOWE, A. G., RICHARDS, C. D. & SCHIRMER, M. (1965) The amount of injected EGTA needed to suppress the contractile response of single Maia muscle fibres and its relation to the amount of calcium released during contraction. J. Physiol. 179, 32–33.Google Scholar
  2. ASHLEY, C. C., MOISESCU, D. G. & ROSE, R. M. (1974) Kinetics of calcium during contraction: myofibrillar and SR fluxes during a single response of a skeletal muscle fibre. In Calcium binding proteins (edited by DRABIKOWSKI, W., STRZELECKA-GOLASZEWSKA, M. & CARAFOLI, E.) pp. 609–42. Amsterdam: Elsevier.Google Scholar
  3. BAKKER, A. J., HEAD, S. I. & STEPHENSON, D. G. (1997) Time course of calcium transients derived from Fura-2 fluorescence measurements in single fast twitch fibres of adult mice and rat myotubes developing in primary culture. Cell Calcium 21, 359–64Google Scholar
  4. BAYLOR, S. M., CHANDLER, W. K. & MARSHALL, M. W. (1983) Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from arsenazo III calcium transients J. Physiol. 344, 625–66.Google Scholar
  5. BLINKS, J. R., RÜDEL, R. & TAYLOR, S. R. (1978) Calcium transients in isolated amphibian muscle fibres: detection with aequorin. J. Physiol. 277, 291–323.Google Scholar
  6. CARDOSO, C. M. & DE MEIS, L. (1993) Modulation by fatty acids of Ca2+ fluxes in sarcoplasmic reticulum vesicles. Biochem. J. 296, 49–52.Google Scholar
  7. CARAFOLI, E. (1987) Intracellular calcium homeostasis Ann. Rev. Biochem. 56, 395–433.Google Scholar
  8. CARROLL, S. L., KLEIN, M. G. & SCHNEIDER, M. F. (1995) Calcium transient in intact rat skeletal muscle fibers in agarose gel. Am. J. Physiol. 269, C28–34.Google Scholar
  9. CHACON, E., OHATA, H., HARPER, I. S., TROLLINGER, D. R., HERMAN, B. & LEMASTERS, J. J. (1996) Mitochondria free calcium transients during excitation-contraction coupling in rabbit cardiac myocytes. FEBS Lett. 382, 31–6.Google Scholar
  10. CLOSE, R. I. (1972) Dynamic properties in mammalian skeletal muscles. Physiol. Rev. 52, 129–97.Google Scholar
  11. CROMPTON, N., SIGEL, E., SALZMANN, M. & CARAFOLI, E. (1976) A kinetic study of the energy-linked influx of Ca2+ into heart mitochondria Eur. J. Biochem. 69, 429–34.Google Scholar
  12. DELBONO, O. & STEPHANI, E. (1993) Calcium transients in single mammalian skeletal muscle fibres. J. Physiol. 463, 689–707.Google Scholar
  13. FRYER, M. W. & NEERING, I.R. (1989) Actions of caffeine on fast and slow twitch muscles of the rat. J. Physiol. 416, 435–54.Google Scholar
  14. GEORGE, J. C. & BERGER, A. J. (1966) Avian Myology. New York: Academic Press.Google Scholar
  15. GILLIS, J. M. (1985) Relaxation of vertebrate skeletal muscle. A synthesis of the biochemical and physiological approaches Biophys. Biochim. Acta 811, 97–145.Google Scholar
  16. GILLIS, J. M., MAES, M. & VERELLEN-DUMOULIN, C. (1973) Controlled application of calcium to sarcolemma-free muscle fibres J. Physiol. 232, 1–3P.Google Scholar
  17. GUNTER, T. E. & PFEIFFER, D. R. (1990) Mechanisms by which mitochondria transport calcium Am. J. Physiol. 258, C755–86.Google Scholar
  18. HAJNÓCZKY, G., ROBB-GASPERS, L. D., SEITZ, M. B. & THOMAS, A. P. (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415–24.Google Scholar
  19. LÄNNERGREN, J. (1971) The effect of low level activation on the mechanical properties of isolated frog muscle fibers. J. Gen. Physiol. 58, 145–62.Google Scholar
  20. MOENS, P., PARTRIDGE, T. A., MORGAN, J. E., BECKERSBLEUKS, G. & MARÉCHAL, G. (1992) Regeneration after free muscle grafting in normal and dystrophic (mdx) mice. J. Neurol. Sci. 111, 209–13.Google Scholar
  21. MOORE, C. L. (1971) Specific inhibition of mitochondrial Ca2+ transport by ruthenium red. Biochem. Biophys. Res. Com., 42, 298–305.Google Scholar
  22. PODOLSKY, R. J. (1964) The maximum sarcomere length for contraction of isolated myofibrils J. Physiol. 170, 110–23.Google Scholar
  23. RIZZUTO, R., SIMPSON, A. W. M., BRINI, M. & POZZAN, T. (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature, 358325–7.Google Scholar
  24. RUTTER, G. A., THELER, J. M., MURGIA, M., WOLLHEIM, C. B., POZZAN, T. & RIZZUTO, R. (1993) Stimulated Ca2+ influx raises mitochondrial free Ca2+ to supramicromolar levels in pancreatic β-cell line. J. Biol. Chem. 268, 22385–90.Google Scholar
  25. SCIOTE, J. J. & KENTISH, J. C. (1996) Unloaded shortening velocities of rabbit masseter muscle fibres expressing skeletal or α-cardiac myosin heavy chains. J. Physiol. 492, 659–67.Google Scholar
  26. WESTERBLAD, H. & ALLEN, D. G. (1991) Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol. 98, 615–35.Google Scholar
  27. WESTERBLAD, H. & ALLEN, D. G. (1995) Relaxation, [Ca2+]i and [Mg2+]i during prolonged tetanic stimulation of intact, single fibres from mouse skeletal muscle. J. Physiol. 480, 31–43.Google Scholar
  28. WOLEDGE, R. C., CURTIN, N. A. & HOMSHER, E. (1985) In Energetics Aspects of Muscle Contraction. Monographs of the Physiol. Soc, 41, pp. 97–8. London: Academic Press.Google Scholar

Copyright information

© Chapman and Hall 1997

Authors and Affiliations

  • J. M. GILLIS
    • 1
  1. 1.Department of PhysiologyCatholic University of Louvain, Faculty of Medicine, UCL 5540BruxellesBelgium

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