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Caffeine-induced calcium release from isolated sarcoplasmic reticulum of rabbit skeletal muscle

  • Excitable Tissues And Central Nervous Physiology
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Abstract

The essential conditions for the Ca2+ releasing action of caffeine from isolated sarcoplasmic reticulum (SR) of rabbits were evaluated by an investigation into the effects of Ca2+, Mg2+, MgATP2−, and ATP concentration, ionic strength, and degree of loading. The heavy fraction (4,500×g) of the reticulum was used. Except for the study on degree of loading, 0.2 mg protein·ml−1 SR was loaded actively with 0.02 mM45CaCl2, resulting in >90 nmol·mg protein−1 at steady state, and then the effects of various parameters with or without (control) caffeine were tested.

It was found that (1) caffeine induces a transient, dosedependent release of Ca2+, (2) the absolute amount of Ca2+ released by caffeine increases with the Ca2+ load of the SR, (3) increasing the ionic strength (μ) from 0.09 to 0.3 lowers the threshold concentration of caffeine, (4) the SR is refractory to a repeated challenge by a caffeine concentration causing maximal effect, (5) caffeine-induced Ca2+ release increases with increasing (a) external Ca2+ concentrations up to 5 μM total Ca2+ (or 3 μM free Ca2+) and (b) free ATP concentrations up to 0.45 mM, and (6) caffeine-induced Ca2+ release is not affected by changes of either the Mg2+ or the MgATP2− concentration.

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References

  1. Endo M (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle. Proc Jpn Acad 51:479–484

    Google Scholar 

  2. Fairhurst AS, Hasselbach W (1970) Calcium efflux from a heavy sarcotubular fraction: Effects of ryanodine, caffeine and magnesium. Eur J Biochem 13:504–509

    Google Scholar 

  3. Feher JJ, Briggs N (1982) The effect of calcium load on the calcium permeability of sarcoplasmic reticulum. J Biol Chem 257:10191–10199

    Google Scholar 

  4. Ford LE, Podolsky RJ (1970) Regenerative calcium release within muscle cells. Science (Wash DC) 167:58–59

    Google Scholar 

  5. Hasselbach W, Makinose M (1963) Über den Mechanismus des Calciumtransportes durch die Membranen des sarkoplasmatischen Reticulums. Biochem Z 339:94–111

    Google Scholar 

  6. Hasselbach W (1966) Structural and enzymatic properties of the calcium transporting membranes of the sarcoplasmic reticulum. Ann New York Acad Sci 137:1041–1048

    Google Scholar 

  7. Hasselbach W, Fiehn W, Makinose M, Migala AJ (1969) Calcium fluxes across isolated sarcoplasmic membranes in the presence and absence of ATP. In: Tosteson DC (ed) The molecular basis of membrane function. Prentice-Hall, Inc, Englewood Cliffs, New Jersey, pp 299–316

    Google Scholar 

  8. Hasselbach W (1979) The sarcoplasmic calcium pump. A model of energy transduction in biological membranes, In: Boschke FL (ed) Topics in current chemistry, vol 78. Springer, Berlin Heidelberg New York, pp 1–56

    Google Scholar 

  9. Hasselbach W, Oetliker H (1983) Energetics and electrogenicity of the sarcoplasmic reticulum calcium pump. Ann Rev Physiol 45:325–339

    Google Scholar 

  10. Inesi G, Malan N (1976) Mechanisms of calcium release in sarcoplasmic reticulum. Life Sci 18:773–779

    Google Scholar 

  11. Johnson PN, Inesi G (1969) The effect of methylxanthines and local anaesthetics on fragmented sarcoplasmic reticulum. J Pharmacol Exp Ther 169:308–314

    Google Scholar 

  12. Kasai M, Kanemasa T, Fukumoto S (1979) Determination of reflection coefficients for various ions and neutral molecules in sarcoplasmic reticulum vesicles through osmotic volume change studied by stopped flow technique. J Membr Biol 51:311–324

    Google Scholar 

  13. Katz AM, Repke DI, Hasselbach W (1977) Dependence of ionophore- and caffeine-induced calcium release from sarcoplasmic reticulum vesicles on external and internal calcium ion concentrations. J Biol Chem 252:1938–1949

    Google Scholar 

  14. Katz AM, Repke DI, Fudyma G, Shigekawa M (1977) Control of calcium efflux from sarcoplasmic reticulum vesicles by external calcium. J Biol Chem 252:4210–4214

    Google Scholar 

  15. Kerrick WGL, Donaldson SKB (1972) The effects of Mg2+ on submaximum Ca2+-activated tension in skinned fibers of frog skeletal muscle. Biochim Biophys Acta 275:117–122

    Google Scholar 

  16. Lüttgau HC, Oetliker H (1968) The action of caffeine on the activation of the contractile mechanism in striated muscle fibers. J Physiol 194:51–74

    Google Scholar 

  17. Martell AE, Schwarzenbach G (1956) Adenosinphosphat und Triphosphat als Komplexbildner für Calcium und Magnesium. Helv Chim Acta 39:653–661

    Google Scholar 

  18. de Meis L, Hasselbach W (1971) Acetylphosphate as substrate for Ca2+ uptake in skeletal muscle microsomes. J Biol Chem 246:4759–4763

    Google Scholar 

  19. Millman MS, Azari J (1977) Adenosine triphosphate-induced rapid calcium release from fragmented sarcoplasmic reticulum. Biochem Biophys Res Comm 78:60–66

    Google Scholar 

  20. Miyamoto H, Racker E (1981) Calcium-induced calcium release at terminal cisternae of skeletal sarcoplasmic reticulum. FEBS Letters 133:235–238

    Google Scholar 

  21. Miyamoto H, Racker E (1982) Mechanism of calcium release from skeletal sarcoplasmic reticulum. J Membr Biol 66:193–201

    Google Scholar 

  22. Mobley BA, Eisenberg BR (1975) Sizes of components of frog skeletal muscle measured by methods of stereology. J Gen Physiol 66:31–45

    Google Scholar 

  23. Nagasaki K, Kasai M (1981) Calcium-induced calcium release from sarcoplasmic reticulum vesicles. J Biochem 90:749–755

    Google Scholar 

  24. Ogawa Y, Kurebayashi N, Harafuji H (1981) Mechanism of Ca release from fragmented sarcoplasmic reticulum from bull frog skeletal muscle. In: Ohnishi ST, Endo M (eds) The mechanism of gated calcium transport across biological membranes. Academic Press Inc, pp 265–273

  25. Robertson SP, Johnson JD, Potter JD (1981) The time-course of Ca2+ exchange with calmodulin, troponin, parvalbumin, and myosin in response to transient increases in Ca2+. Biophys J 34:559–569

    Google Scholar 

  26. Sandow A, Brust M (1966) Caffeine potentiation of twitch tension in frog sartorius muscle. Biochemische Zeitschrift 345:232–247

    Google Scholar 

  27. Schwarzenbach G, Senn H, Anderegg G (1957) Komplexone XXIX. Ein großer Chelateffekt besonderer Art. Helv Chim Acta 40:1886–1900

    Google Scholar 

  28. Somlyo AV, Gonzalez-Serratos H, Shuman H, McClellan G, Somlyo AP (1981) Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: An electron probe study. J Cell Biol 90:577–594

    Google Scholar 

  29. Stephenson EW, Podolsky RJ (1977) Regulation by magnesium of intracellular calcium movement in skinned muscle fibers. J Gen Physiol 69:1–16

    Google Scholar 

  30. Stephenson EW (1981) Ca2+ dependence of stimulated45Ca efflux in skinned muscle fibers. J Gen Physiol 77:419–443

    Google Scholar 

  31. Swoboda G, Hasselbach W (1982) Bile salt delipidation, residual phaspholipids and reactivation of the Ca2+ ATPase from sarcoplasmic reticulum. Z Naturforsch 37c:289–298

    Google Scholar 

  32. Waas W, Hasselbach W (1981) Interference of nucleoside diphosphates and inorganic phosphate with nucleoside-triphosphate-dependent calcium fluxes and calcium-dependent nucleoside-triphosphate hydrolysis in membranes of sarcoplasmic-reticulum vesicles. Eur J Biochem 116:601–608

    Google Scholar 

  33. Weber A, Herz R (1968) The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol 52:750–759

    Google Scholar 

  34. Weber A (1968) The mechanism of the action of caffeine on sarcoplasmic reticulum. J Gen Physiol 52:760–772

    Google Scholar 

  35. Weber A, Murray JM (1973) Molecular control mechanisms in muscle contraction. Physiol Rev 53:612–673

    Google Scholar 

  36. Yamamoto N, Kasai M (1982) Kinetics of the actions of caffeine and procaine on the Ca2+-gated cation channel in sarcoplasmic reticulum vesicles. J Biochem 92:477–484

    Google Scholar 

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Authors and Affiliations

  1. Department of Anesthesiology, RN-10, University of Washington, 98195, Seattle, WA, USA

    Judy Y. Su (Visiting scientist)

  2. Max-Planck-Institut für Medizinische Forschung, D-6900, Heidelberg, Federal Republic of Germany

    Wilhelm Hasselbach

Authors
  1. Judy Y. Su
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  2. Wilhelm Hasselbach
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Su, J.Y., Hasselbach, W. Caffeine-induced calcium release from isolated sarcoplasmic reticulum of rabbit skeletal muscle. Pflugers Arch. 400, 14–21 (1984). https://doi.org/10.1007/BF00670530

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  • DOI: https://doi.org/10.1007/BF00670530

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