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.
Similar content being viewed by others
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.
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.
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.
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.
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.
Endo, M. (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle.Proc. Jpn. Acad. 51, 479–84.
Endo, M. &Nakajima, Y. (1973) Release of calcium induced by ‘depolarisation’ of the sarcoplasmic reticulum membrane.Nature (Lond.) New Biol. 246, 216–18.
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.
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.
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.
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.
Garcia, A. M. &Miller, C. (1984) Channel-mediated monovalent cation fluxes in isolated sarcoplasmic reticulum vesicles.J. gen. Physiol. 83, 819–939.
Gattass, C. R. &De Meis, L. (1978) The mechanism by which quinine inhibits the Ca2+ transport of sarcoplasmic reticulum.Biochem. Pharmacol. 27, 539–45.
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.
Hasselbach, W. &Oetliker, H. (1983) Energetics and electrogenecity of the sarcoplasmic reticulum calcium pump.Ann. Rev. Physiol. 45, 325–39.
Isaacson, A. &Sandow, A. (1967) Quinine and caffeine effects on45Ca movements in frog sartorius muscle.J. gen. Physiol. 50, 2109–28.
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.
Kitazawa, T. &Endo, M. (1976) Increase in passive calcium influx into the sarcoplasmic reticulum by ‘depolarization’ and caffeine.Proc. Jpn. Acad. 52, 599–602.
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.
Kitazawa, T., Shuman, H. &Somlyo, A. P. (1983) Quantitative electron probe analysis: Problems and solutions.Ultramicroscopy 11, 251–62.
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.
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.
Meissner, G. (1983) Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum.Molec. cell. Biochem. 55, 65–82.
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.
Ogawa, Y. (1970) Some properties of frog fragmented sarcoplasmic reticulum with particular reference to its response to caffeine.J. Biochem. (Tokyo) 67, 667–83.
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.
Pang, D. C. &Briggs, F. N. (1976) Mechanism of quinidine and chlorpromazine inhibition of sarcotubular ATPase activity.Biochem. Pharmacol. 25, 21–5.
Sakai, T., Geffner, E. S. &Sandow, A. (1971) Caffeine contracture in muscle with disrupted transverse tubules.Amer. J. Physiol. 220, 712–19.
Salama, G. &Scarpa, A. (1985) Magnesium permeability of sarcoplasmic reticulum.J. biol. Chem. 260, 11697–705.
Shuman, H., Somlyo, A. V. &Somlyo, A. P. (1976) Quantitative electron probe microanalysis of biological thin sections: Methods and validity.Ultramicroscopy 1, 317–39.
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.
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.
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.
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.
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.
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.
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.
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.
Weber, A. (1968) The mechanism of action of caffeine in sarcoplasmic reticulum.J. gen. Physiol. 52, 760–72.
Worsfold, M. &Peter, J. B. (1970) Kinetics of calcium transport by fragmented sarcoplasmic reticulum.J. biol. Chem. 245, 5545–52.
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.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01568888