Skip to main content
Log in

Non-homogeneous Ca release in isolated frog skeletal muscle fibres

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

We have examined the spatial distribution of [Ca2+]i during tetanic stimulation in frog skeletal muscle cells using a fluorescence imaging method. We have found a completely unexpected pattern of Ca release: Ca is released forming gradients composed of spots of very significant and slow fluctuations of calcium release. Our findings could be explained if the calcium release process in skeletal muscle is influenced significantly by [Ca2+]i, such as in cardiac muscle, and suggests that the SR/Ca release control can include the established voltage-dependent plus a cardiac-like process of calcium-induced Ca release and a Ca release inhibition by Ca.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • BAYLOR, S. M., CHANDLER, W. K. & MARSHALL, M. W. (1979) Arsenazo II signals in singly dissociated frog twitch fibres. J. Physiol. 287, 23P-24P.

    Google Scholar 

  • 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 

  • BERLIN, J. R., CANNELL, M. B. & LEDERER, W. J. (1989) Cellular origins of the transient inward current in cardiac myocytes. Role of fluctuations and waves of elevated intracellular calcium. Circ. Res. 65, 115–26.

    Google Scholar 

  • Blinks, J. R. (1965) Influence of osmotic strength on cross-section and volume of isolated single muscle fibres. J. Physiol. 177, 42–57.

    Google Scholar 

  • BREHM, P., LECHLEITER, J., SMITH, S. & DUNLAP, K. (1989) Intracellular signaling as visualized by endogenous calcium-dependent bioluminescence. Neuron 3, 191–8.

    Google Scholar 

  • CANNELL, M. B. & ALLEN, D. G. (1984) Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys. J. 45, 913–25.

    Google Scholar 

  • ELZINGA, G., HOWARTH, J. V., RALL, J. A., WILSON, M. G. A. & WOLEDGE, R. C. (1989) Variation in the normalized tetanic force of single frog muscle fibres. J. Physiol. 410, 157–70.

    Google Scholar 

  • ENDO, M., TANAKA, M. & OGAWA, Y. (1970) Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibers. Nature 228, 34–6.

    Google Scholar 

  • HIROTA, A., CHANDLER, W. K., SOUTHWICK, P. L. & WAGGONER, A. S. (1989) Calcium signals recorded from two new purpurate indicators inside frog cut twitch fibers. J. Gen. Physiol. 94, 597–631.

    Google Scholar 

  • HORIUTI, K., HIGUCHI, H., UMAZUME, Y., KONISHI, M., OKAZAKI, O. & KURIHAI, S. (1988) Mechanism of action of 2,3-butanedione 2-monoxime on contraction of frog skeletal muscle fibres. J. Muscle Res. Cell Motil. 9, 156–64.

    Google Scholar 

  • Klein, M. G., Simon, B. J., Szucs, G. & Schneider, M. F. (1988) Simultaneous recording of calcium transients in skeletal muscle using high-and low-affinity calcium indicators. Biophys. J. 53, 971–88.

    Google Scholar 

  • LECHLEITER, J., GIRARD, S., PERALTA, E. & CLAPHAM, D. (1991) Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. Science 252, 123–6.

    Google Scholar 

  • LIPSCOMBE, D., MADISON, D. V., POENIE, M., REUTER, H., TSIEN, R. Y. & TSIEN, R. W. (1988) Spatial distribution of calcium channels and cytosolic calcium transient in growth cones and cell bodies of sympathetic neuron. Proc. Natl. Acad. Sci. 85, 2398–402.

    Google Scholar 

  • MA, J., FILL, M., KNUDSON, C. M., CAMPBELL, K. P. & CORONADO, R. (1988) Ryanodine receptor of skeletal muscle is a gap junction-type channel. Science 242, 99–102.

    Google Scholar 

  • MEISSNER, G. & HENDERSON, J. S. (1987) Rapid calcium release from cardiac sarcoplasmic reticulum vesicles is dependent on Ca2+ and is modulated by Mg2+ adenine nucleotide, and calmodulin. J. Biolog. Chem. 262, 3065–73.

    Google Scholar 

  • MILEDI, R., PARKER, I. & ZHU, P. H. (1982) Calcium transients evoked by action potentials in frog twitch muscle fibres. J. Physiol. 333, 655–79.

    Google Scholar 

  • MONCK, J. R., OBERHAUSER, A. F., KEATING, T. J. & FERNANDEZ, J. M. (1992) Thin-section ratiometric Ca2+ images obtained by optical sectioning of Fura-2 loaded mast cells. J. Cell Biol. 116, 745–59.

    Google Scholar 

  • NEERING, I. R., QUESENBERRY, L. A., MORRIS, V. A. & TAYLOR, S. R. (1991) Nonuniform volume changes during muscle contraction. Biophys. J. 59, 926–32.

    Google Scholar 

  • NIGGLI, E. & LEDERER, W. J. (1990a) Voltage-independent calcium release in heart muscle. Science 250, 565–8.

    Google Scholar 

  • NIGGLI, E. & LEDERER, W. J. (1990b) Real-time confocal microscopy and calcium measurements in heart muscle cells towards the development of a fluorescence microscope with high temporal and spatial resolution. Cell Calcium 11, 121–30.

    Google Scholar 

  • PAPE, P., KONISHI, M., HOLLINGWORTH, S. & BAYLOR, S. M. (1990) Perturbation of sarcoplasmic reticulum calcium release and phenol red absorbance transients by large concentration of Fura-2 injected into frog skeletal muscle fibers. J. Gen. Physiol. 96, 493–516.

    Google Scholar 

  • PEACHY, L. D. & EISENBERG, B. R. (1978) Helicoids in the T system and striations of frog skeletal muscle fibers seen by high voltage electron microscope. Biophys. J. 22, 145–54.

    Google Scholar 

  • ROUSSEAU, E. & PINKOS, J. (1990) pH modulates conducting and gating behaviour of single calcium release channels. Pflüger's Arch. 415, 645–7.

    Google Scholar 

  • SCHNEIDER, M. F. & SIMON, B. J. (1988) Inactivation of calcium release from the sarcoplasmic reticulum in frog skeletal muscle. J. Physiol. 405, 727–45.

    Google Scholar 

  • SHARNOFF, M., KARCHER, T. H. & BREHM, L. P. (1984) Microdifferential holography and the polysarcomeric unit of activation of skeletal muscle. Science 223, 822–5.

    Google Scholar 

  • SOMLYO, A. V., GONZALEZ-SERRATOS, H., SHUMAN, H., McClellan, G. & Somlyo, A. P. (1981) Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: An electron-probe study. J. Cell Biol. 90, 577–94.

    Google Scholar 

  • TANABE, T., BEAM, K. G., ADAMS, B. A., NIIDOME, T. & NUMA, S. (1990) Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 346, 567–9.

    Google Scholar 

  • VAN DERKLOOT, W. G. (1969) The steps between depolarization and the increase in the respiration of frog skeletal muscle. J. Physiol. 204, 551–69.

    Google Scholar 

  • VERGARA, J., DIFRANCO, M., COMPAGNON, D. & SUAREZ-ISLA, B. A. (1991) Imaging of calcium transients in skeletal muscle fibers. Biophys. J. 59, 12–24.

    Google Scholar 

  • WESTERBLAD, H., LEE, J. A., LAMB, A. G., BOLSOVER, S. R. & ALLEN, D. G. (1990) Spatial gradients of intracellular calcium in skeletal muscle during fatigue. Pflüger's Arch. 415, 734–40.

    Google Scholar 

  • WROGEMANN, K. & PENA, S. D. J. (1976) Mitochondrial calcium overload: a general mechanism for cell necrosis in muscle diseases. Lancet 27, 672–3.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rozycka, M., Gonzalez-Serratos, H. & Goldman, W. Non-homogeneous Ca release in isolated frog skeletal muscle fibres. J Muscle Res Cell Motil 14, 527–532 (1993). https://doi.org/10.1007/BF00297215

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00297215

Keywords

Navigation