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The effects of chloride ions in excitation-contraction coupling and sarcoplasmic reticulum calcium release in twitch muscle fibre

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Summary

Using the sucrose vaseline gap technique, experiments were carried out on isolated frog twitch muscle fibre to investigate the role of chloride ions in excitation-contraction coupling. In current clamp conditions, replacement of chloride ions by impermeant anions led to an increase of the amplitude of the early after potential and of the amplitude of the twitch. Addition of a chloride channel blocker, anthracene-9-carboxylic acid gave similar results. In voltage clamp conditions, replacement of chloride ions by impermeant anions induced a decrease of the outward current and an increase of both the amplitude of the contraction and of the resting tension. Addition of anthracene-9-carboxylic acid gave similar results except that resting tension was not modified. Replacement of chloride ions by impermeant anions resulted in a shift of the tension-voltage relationship toward negative potentials and in an incrase of the amplitude of the contraction at all potentials. Outward currents were also reduced at all potentials but no shift of the current-voltage relationship was observed. Similar results were obtained upon addition of anthracene-9-carboxylic acid. Rapid filtration experiments were performed on isolated sarcoplasmic reticulum vesicles to study the role of chloride ions in Ca2+ release. Under conditions where KCl was present in the intra- and extravesicular media, removal of chloride ions from the release solution produced a 2-fold increase in the rate of Ca2+-induced Ca2+ release. Together, these results suggest that, besides their involvement in the action potential time course, chloride ions could exert a negative control on the sarcoplasmic reticulum Ca2+ release. A reduced entry of chloride ions in the triadic junctional restricted compartment is capable of creating a chloride gradient across the sarcoplasmic reticulum membrane facilitating the sarcoplasmic reticulum release.

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References

  • ABRAMCHECK, C. W. & BEST, P. M. (1989). Physiological role and selectivity of the in situ potassium channel of the sarcoplasmic reticulum in skinned frog skeletal muscle fibers. J. Gen. Physiol. 93, 1–21.

    Google Scholar 

  • ADRIAN, R. H. & FREYGANG, W. H. (1962) The potassium and chloride conductance of frog muscle membrane. J. Physiol. 163, 61–103.

    Google Scholar 

  • ALLARD, B & ROUGIER, O. (1992a). Reappraisal of the role of sodium ions in excitation-contraction coupling in frog, twitch muscle. J. Muscle Res. Cell. Motil. 13, 117–25.

    Google Scholar 

  • ALLARD, B. & ROUGIER, O. (1992b). Rôle des ions chlorure dans le couplage excitation-contraction de la fibre musculaire squelettique rapide de grenouille. Arch. Int. Physiol. Biochem. Biophys. 100, A78.

    Google Scholar 

  • BOYLE, P. J. & CONWAY, E. J. (1941). Potassium accumulation in muscle and associated changes. J. Physiol. 100, 1–63.

    Google Scholar 

  • BREGAT, A. H., DAWE, S. R. & MOSKWA, A. G. (1980). Chemically induced myotania in amphibia. Nature 286, 625–6.

    Google Scholar 

  • BRYANT, S. H. & MORALES-AGUILERA, A. (1971). Chloride conductance in normal and myotonic fibres and the action of monocarboxylic aromatic acid. J. Physiol. 219, 367–83.

    Google Scholar 

  • CAILLE, J., ILDEFONSE, M. & ROUGIER, O. (1978). Existence of a sodium current in the tubular membrane of frog twitch muscle fibre; its possible role in the activation of contraction of twitch muscle fibre. Plügers Archiv. 374, 167–77.

    Google Scholar 

  • DULHUNTY, A. (1982). Effect of chloride withdrawal on the geometry of the t-tubules in amphibian and mammalian muscle. J. Membrane Biol. 67, 81–91.

    Google Scholar 

  • DUPONT, Y. (1977). Kinetics and regulation of sarcoplasmic reticulum ATPase. Eur. J. Biochem. 72, 185–90.

    Google Scholar 

  • EISENBERG, R. S. & GAGE, P. W. (1969). Ionic conductances of the surface and transverse tubular membranes of frog sartorius fibers. J. Gen. Physiol. 53, 279–97.

    Google Scholar 

  • FALK, G. & LANDA, J. F. (1960). Prolonged response of skeletal muscle in the absence of penetrating anions. Am. J. Physiol. 198, 289–99.

    Google Scholar 

  • FOULKS, J. G., PACEY, J. A. & PERRY, F. A. (1965). Contractures and swelling of the transverse tubules during chloride withdrawal in frog skeletal muscle. J. Physiol. 180, 96–115.

    Google Scholar 

  • FRANZINI-ARMSTRONG, C. & NUNZI, G. (1983). Junctional feet and particles in the triads of a fast twitch muscle fiber. J. Muscle Res. Cell Motil. 4, 233–52.

    Google Scholar 

  • GARCIA, A. M. & MILLER, C. (1984). Channel-mediated monovalent cation fluxes in isolated sarcoplasmic reticulum vesicles. J. Gen. Physiol. 83, 819–39.

    Google Scholar 

  • GORDON, A. M. & GODT, R. E. (1970). Some effects of hypertonic solutions on contraction and excitation-contraction coupling in frog skeletal muscles. J. Gen. Physiol. 55, 254–75.

    Google Scholar 

  • HASSELBACH, W. & MAKINOSE, M. (1963). Ueber den Mechanismus des Calcium-transportes durch die Membranen des Sarkoplasmatischen Reticulums. Biochem. Zeitschr. 339, 94–111.

    Google Scholar 

  • HEINY, J. A., VALLE, J. R. & BRYANT, S. H. (1990). Optical evidence for a chloride conductance in the T-system of frog skeletal muscle. Pflügers Arch. 416, 288–95.

    Google Scholar 

  • HILL, A. V. & HOWARTH, J. V. (1957). The effect of potassium on the resting metabolism of the frog's sartorius. Proc. Royal Soc. Lon. B 147, 21–43.

    Google Scholar 

  • HODGKIN, A. L. & HOROWICZ, P. (1959). The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J. Physiol. 148, 127–60.

    Google Scholar 

  • HODKIN, A. L. & HOROWICZ, P. (1960). The effect of sudden changes in ionic concentrations on the membrane potential of single muscle fibres. J. Physiol. 153, 370–80.

    Google Scholar 

  • HUI, C. S. (1991). Factors affecting the appearance of the hump charge movement component in frog cut twitch fibers. J. Gen. Physiol. 98, 315–47.

    Google Scholar 

  • HUTTER, O. F. & NOBLE, D. (1960). The chloride conductance of frog skeletal muscle. J. Physiol. 151, 89–102.

    Google Scholar 

  • HUTTER, O. F. & WARNER, A. E. (1967). The pH sensitivity of the chloride conductance of frog skeletal muscle. J. Physiol. 189, 403–25.

    Google Scholar 

  • IDE, T., SAKAMOTO, H., MORITA, T., TAGUCHI, T. & KASAI, M. (1991). Purification of a Cl- channel protein of sarcoplasmic reticulum by assaying the channel activity in the planar lipid bilayer system. Biochem. Biophys. Res. Commun. 176, 38–44.

    Google Scholar 

  • KAO, C. Y. & STANFIELD, P. R. (1968). Actions of some anions on electrical properties and mechanical threshold of frog twitch muscle. J. Physiol. 198, 291–309.

    Google Scholar 

  • KOMETANI, T. & KASAI, M. (1978). Ionic permeability of sarcoplasmic reticulum vesicles measured by light scattering method. J. Membrane Biol. 41, 295–308.

    Google Scholar 

  • LAMB, G. D., STEPHENSON, D. G. & STIENEN, G. J. M. (1993). Effects of osmolarity and ionic strength on the mechanism of Ca2+ release in skinned skeletal muscle fibres of the toad. J. Physiol. 464, 629–48.

    Google Scholar 

  • McKINELY, D. & MEISSNER, G. (1978). Evidence for a K+, Na+ permeable channel in sarcoplasmic reticulum. J. Membrane Biol. 44, 159–86.

    Google Scholar 

  • MATSUSHIMA, T., FUJINO, M. & NAGAI, T. (1962). Effects of anomalous anions on the caffeine contracture. Japan J. Physiol. 12, 106–12.

    Google Scholar 

  • MEISSNER, G. & McKINLEY, D. (1976). Permeability of sarcoplasmic reticulum membrane. The effect of changed ionic environments on Ca2+ release. J. Membrane Biol. 30, 79–98.

    Google Scholar 

  • MOBLEY, B. A. & EISENBERG, B. R. (1975). Sizes of components in frog skeletal muscle measured by methods of stereology. J. Gen. Physiol. 66, 31–45.

    Google Scholar 

  • MOUTIN, J. J. & DUPONT, Y. (1988). Rapid filtration studies of Ca2+-induced Ca2+ release from skeletal sarcoplasmic reticulum. J. Biol. Chem. 263, 4228–35.

    Google Scholar 

  • PALADE, P. T. & BARCHI, R. L. (1977). On the inhibition of muscle membrane chloride conductance by aromatic carboxylic acids. J. Gen. Physiol. 69, 879–96.

    Google Scholar 

  • PORTREAU, D. & RAYMOND, G. (1980). Slow inward Barium current and contraction on frog single muscle fibres. J. Physiol. 303, 91–109.

    Google Scholar 

  • RÜDEL, R. & LEHMANN-HORN, F. (1985). Membrane changes in cells from myotonia patients. Physiol. Rev. 65, 310–56.

    Google Scholar 

  • SOLANDT, D. Y. (1936). The effect of potassium on the excitability and resting metabolism of frog's muscle. J. Physiol. 86, 162–70.

    Google Scholar 

  • SOMLYO, A. V., GONZALES-SERRATOS, H., SCHUMAN, H., McCLELLAN, G. & SOMLYO, A. P. (1981). Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron probe study. J. Cellular Biol. 90, 577–94.

    Google Scholar 

  • SOMLYO, A. V., SCHUMAN, H. & SOMLYO, A. P. (1977). Composition of sarcoplasmic reticulum in situ by electron probe X-ray microanalysis. Nature 268, 556–8.

    Google Scholar 

  • SZÜCS, G., CSERNOCK, L., MAGYAR, J. & KOVACS, L. (1991). Contraction threshold and the ‘hump’ component of charge movement in frog skeletal muscle. J. Gen. Physiol. 97, 897–911.

    Google Scholar 

  • VIANNA (1975). Interaction of calcium and magnesium in activating and inhibiting the nucleotide triphosphatase of sarcoplasmic reticulum vesicles. Biochim. Biophys. Acta 410, 389–406.

    Google Scholar 

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Allard, B., Rougier, O. The effects of chloride ions in excitation-contraction coupling and sarcoplasmic reticulum calcium release in twitch muscle fibre. J Muscle Res Cell Motil 15, 563–571 (1994). https://doi.org/10.1007/BF00121162

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  • DOI: https://doi.org/10.1007/BF00121162

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