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The effects of quinine on the calcium and magnesium content of the sarcoplasmic reticulum and the temperature-dependence of quinine contractures

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Summary

A significant decrease in the Ca2+ and increase in the Mg2+ content of the terminal cisternae (TC) of the sarcoplasmic reticulum (SR) during quinine contraction was demonstrated by electron probe analysis of rapidly frozen frog muscles. The extent of Ca2+ release (71% of total) from the TC and the absence of an increase in total cell Ca2+ support the conclusion that quinine contractures are caused by passive efflux of Ca2+ from the SR when the latter is uncompensated due to inhibition of the SR Ca2+ pump by quinine. A rapid warming contraction (RWC) was observed, in the presence of quinine, when the temperature of intact and skinned muscles was increased from about 5° C to 18–23° C. The duration of the latency of quinine contracture, in intact muscle bundles, was approximately 31 s at 3° C and 2 s at 23° C. The results suggest a significant temperature sensitivity of the passive Ca2+ channels of the SR membrane, although an effect of temperature on the lipid partition coefficient of quinine into the SR has not been ruled out.

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References

  • Andersson, K. E. (1972) Effects of chlorpromazine, imipramine, and quinidine on the mechanical activity of single skeletal muscle fibres of the frog.Acta Physiol. Scand 85, 532–46.

    PubMed  Google Scholar 

  • Balzer, H. (1972) The effect of quinidine and drugs with quinidine-like action (propanolol, verapamil and tetracaine) on the calcium transport system in isolated sarcoplasmic reticulum vesicles of rabbit skeletal muscle.Naunyn-Schmiedebergs Archs. Pharmacol. 274, 256–72.

    Google Scholar 

  • Carvalho, A. P. (1968) Calcium-binding properties of sarcoplasmic reticulum as influenced by ATP, caffeine, quinine, and local anaesthetics.J. gen. Physiol. 52, 622–42.

    PubMed  Google Scholar 

  • Chamberlain, B. K., Volpe, P. &Fleischer, S. (1984) Inhibition of calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles.J. biol. Chem. 259, 7547–53.

    PubMed  Google Scholar 

  • Eletr, S. &Inesi, G. (1972) Phase changes in the lipid moieties of sarcoplasmic reticulum membranes induced by temperature and protein conformational changes.Biochim. biophys. Acta 290, 178–85.

    PubMed  Google Scholar 

  • Endo, M. (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle.Proc. Jpn. Acad. 51, 479–84.

    Google Scholar 

  • Endo, M. &Nakajima, Y. (1973) Release of calcium induced by ‘depolarisation’ of the sarcoplasmic reticulum membrane.Nature (Lond.) New Biol. 246, 216–18.

    Google Scholar 

  • Feher, J. J. &Briggs, F. N. (1982) The effect of calcium load on the calcium permeability of sarcoplasmic reticulum.J. biol. Chem. 257, 10191–99.

    PubMed  Google Scholar 

  • Franciolini, F. (1984) Effects of quinine on the isometric tension and intracellular calcium movements in single giant muscle fibres.Acta Physiol. Hung. 63, 147–51.

    PubMed  Google Scholar 

  • Fuchs, F., Gertz, E. W. &Briggs, F. N. (1968) The effect of quinidine on calcium accumulation by isolated sarcoplasmic reticulum of skeletal and cardiac muscle.J. gen. Physiol. 52, 955–68.

    PubMed  Google Scholar 

  • Fuchs, F., Hartshorne, D. J. &Barns, E. M. (1974) ATPase activity and superprecipitation of skeletal muscle actomyosin of frog and rabbit: Effect of temperature on calcium sensitivity.Comp. Biochem. Physiol. 51B, 165–70.

    Google Scholar 

  • Garcia, A. M. &Miller, C. (1984) Channel-mediated monovalent cation fluxes in isolated sarcoplasmic reticulum vesicles.J. gen. Physiol. 83, 819–939.

    PubMed  Google Scholar 

  • Gattass, C. R. &De Meis, L. (1978) The mechanism by which quinine inhibits the Ca2+ transport of sarcoplasmic reticulum.Biochem. Pharmacol. 27, 539–45.

    PubMed  Google Scholar 

  • Hall, T. A. (1971) The microprobe assay of chemical elements. InPhysical Techniques in Biological Research (edited byOster, G.), Vol. 1A, pp. 158–275. New York: Academic Press.

    Google Scholar 

  • Hasselbach, W. &Oetliker, H. (1983) Energetics and electrogenecity of the sarcoplasmic reticulum calcium pump.Ann. Rev. Physiol. 45, 325–39.

    Google Scholar 

  • Isaacson, A. &Sandow, A. (1967) Quinine and caffeine effects on45Ca movements in frog sartorius muscle.J. gen. Physiol. 50, 2109–28.

    PubMed  Google Scholar 

  • Katz, A. M., Repke, D. I., Dunnett, J. &Hasselbach, W. (1977) Dependence of calcium permeability of sarcoplasmic reticulum vesicles on external and internal calcium ion concentrations.J. biol. Chem. 252, 1950–6.

    PubMed  Google Scholar 

  • Kitazawa, T. &Endo, M. (1976) Increase in passive calcium influx into the sarcoplasmic reticulum by ‘depolarization’ and caffeine.Proc. Jpn. Acad. 52, 599–602.

    Google Scholar 

  • Kitazawa, T., Shuman, H. &Somlyo, A. P. (1982) Calcium and magnesium binding to thin and thick filaments in skinned muscle fibres: Electron probe analysis.J. Musc. Res. Cell Motility 3, 437–54.

    Google Scholar 

  • Kitazawa, T., Shuman, H. &Somlyo, A. P. (1983) Quantitative electron probe analysis: Problems and solutions.Ultramicroscopy 11, 251–62.

    Google Scholar 

  • Kitazawa, T., Somlyo, A. P. &Somlyo, A. V. (1984) The effects of valinomycin on ion movements across the sarcoplasmic reticulum in frog muscle.J. Physiol. (London) 350, 253–68.

    Google Scholar 

  • Martonosi, A. &Beeler, T. J. (1983) Mechanism of Ca2+ transport by sarcoplasmic reticulum. InHandbook of Physiology: Skeletal Muscle (edited byPeachey, L. D., Adrian, R. H. andGeiger, S. R.), pp. 417–86. Bethesda, MD: American Physiological Society.

    Google Scholar 

  • Meissner, G. (1983) Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum.Molec. cell. Biochem. 55, 65–82.

    PubMed  Google Scholar 

  • Nagasaki, K. &Kasai, M. (1984) Channel selectivity and gating specificity of calcium-induced calcium release channel in isolated sarcoplasmic reticulum.J. Biochem. (Tokyo) 96, 1769–75.

    Google Scholar 

  • Ogawa, Y. (1970) Some properties of frog fragmented sarcoplasmic reticulum with particular reference to its response to caffeine.J. Biochem. (Tokyo) 67, 667–83.

    Google Scholar 

  • Palade, P., Mitchell, R. D. &Fleischer, S. (1983) Spontaneous calcium release from sarcoplasmic reticulum: general description and effects of calcium.J. biol. Chem. 258, 8098–107.

    PubMed  Google Scholar 

  • Pang, D. C. &Briggs, F. N. (1976) Mechanism of quinidine and chlorpromazine inhibition of sarcotubular ATPase activity.Biochem. Pharmacol. 25, 21–5.

    PubMed  Google Scholar 

  • Sakai, T., Geffner, E. S. &Sandow, A. (1971) Caffeine contracture in muscle with disrupted transverse tubules.Amer. J. Physiol. 220, 712–19.

    PubMed  Google Scholar 

  • Salama, G. &Scarpa, A. (1985) Magnesium permeability of sarcoplasmic reticulum.J. biol. Chem. 260, 11697–705.

    PubMed  Google Scholar 

  • Shuman, H., Somlyo, A. V. &Somlyo, A. P. (1976) Quantitative electron probe microanalysis of biological thin sections: Methods and validity.Ultramicroscopy 1, 317–39.

    PubMed  Google Scholar 

  • Somlyo, A. P., Somlyo, A. V. &Shuman, H. (1979) Electron probe analysis of vascular smooth muscle: Composition of mitochondria, nuclei and cytoplasm.J. Cell Biol. 81, 316–35.

    PubMed  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.

    PubMed  Google Scholar 

  • Somlyo, A. V., Kitazawa, T., Gonzalez-Serratos, H., McClellan, G. &Somlyo, A. P. (1985a) Ion movements associated with Ca release and uptake in the sarcoplasmic reticulum. InCalcium in Biological Systems (edited byRubin, R. P., Weiss, G. andPutney, J. W., Jr.), pp. 351–8. New York: Plenum Press.

    Google Scholar 

  • Somlyo, A. V., McClellan, G., Gonzalez-Serratos, H., McClellan, G. &Somlyo, A. P. (1985b) Electron probe X-ray microanalysis of post-tetanic Ca and Mg movements across the sarcoplasmic reticulumin situ.J. biol. Chem. 260, 6801–7.

    PubMed  Google Scholar 

  • Somlyo, A. V., Shuman, H. &Somlyo, A. P. (1977) Elemental distributions in striated muscle and effects of hypertonicity: Electron probe analysis of cryo sections.J. Cell Biol. 74, 828–57.

    PubMed  Google Scholar 

  • Suarez-Kurtz, G., DaCosta, M. J. B. &Coutinho, S. (1980) Effects of high potassium concentrations and of chloride substitution on the guinine-induced contractures of frog skeletal muscle.J. pharmacol. exp. Therap. 214, 171–8.

    Google Scholar 

  • Uyeki, E. M., Geiling, E. M. K. & DuBois, K. P. (1954) Studies of the effects of quinidine on intermediary carbohydrate metabolism.Archs. Int. Pharmacodyn. 97, 191–205.

    Google Scholar 

  • Volpe, P., Palade, P., Costello, B., Mitchell, R. E. &Fleischer, S. (1983) Spontaneous calcium release from sarcoplasmic reticulum: Effect of local anesthetics.J. biol. Chem. 258, 12434–42.

    PubMed  Google Scholar 

  • Weber, A. (1968) The mechanism of action of caffeine in sarcoplasmic reticulum.J. gen. Physiol. 52, 760–72.

    PubMed  Google Scholar 

  • Worsfold, M. &Peter, J. B. (1970) Kinetics of calcium transport by fragmented sarcoplasmic reticulum.J. biol. Chem. 245, 5545–52.

    PubMed  Google Scholar 

  • Yoshioka, T., Narusawa, M., Nakano, S. &Somlyo, A. P. (1984) Changes in Ca and Mg during quinine contracture in the sarcoplasmic reticulum (SR) of frog muscle. InProceedings of Third International Congress on Cell Biology, p. 514a, Tokyo.

  • Yoshioka, T. &Somlyo, A. P. (1984) The calcium and magnesium contents and volume of the terminal cisternae in caffeine-treated skeletal muscle.J. Cell Biol. 99, 558–68.

    PubMed  Google Scholar 

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Yoshioka, T., Somlyo, A.P. The effects of quinine on the calcium and magnesium content of the sarcoplasmic reticulum and the temperature-dependence of quinine contractures. J Muscle Res Cell Motil 8, 322–328 (1987). https://doi.org/10.1007/BF01568888

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