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The Journal of Membrane Biology

, Volume 90, Issue 3, pp 219–230 | Cite as

Caffeine inhibition of calcium accumulation by the sarcoplasmic reticulum in mammalian skinned fibers

  • M. M. Sorenson
  • H. S. L. Coelho
  • J. P. Reuben
Articles

Summary

Oxalate-supported Ca accumulation by the sarcoplasmic reticulum (SR) of chemically skinned mammalian skeletal muscle fibers is activated by MgATP and Ca2+ and partially inhibited by caffeine. Inhibition by caffeine is greatest when Ca2+ exceeds 0.3 to 0.4 μm, when free ATP exceeds 0.8 to 1mm, and when the inhibitor is present from the beginning of the loading period rather than when it is added after Ca oxalate has already begun to precipitate within the SR. Under the most favorable combination of these conditions, this effect of caffeine is maximal at 2.5 to 5mm and is half-maximal at approximately 0.5mm. For a given concentration of caffeine, inhibition decreases to one-half of its maximum value when free ATP is reduced to 0.2 to 0.3mm. Varying free Mg2+ (0.1 to 2mm) or MgATP (0.03 to 10mm) has no effect on inhibition. Average residual uptake rates in the presence of 5mm caffeine atpCa 6.4 range from 32 to 70% of the control rates in fibers from different animals. The extent of inhibition in whole-muscle homogenates is similar to that observed in skinned fibers, but further purification of SR membranes by differential centrifugation reduces their ability to respond to caffeine. In skinned fibers, caffeine does not alter the Ca2+ concentration dependence of Ca uptake (K0.5, 0.5 to 0.8 μm; Hilln, 1.5 to 2.1). Reductions in rate due to caffeine are accompanied by proportional reductions in maximum capacity of the fibers, and this configuration can be mimicked by treating fibers with the ionophore A23187. Caffeine induces a sustained release of Ca from fibers loaded with Ca oxalate. However, caffeine-induced Ca release is transient when fibers are loaded without oxalate. The effects of caffeine on rate and capacity of Ca uptake as well as the sustained and transient effects on uptake and release observed under different conditions can be accounted for by a single mode of action of caffeine: it increases Ca permeability in a limited population of SR membranes, and these membranes coexist with a population of caffeine-insensitive membranes within the same fiber.

Key Words

chemically skinned fibers caffeine Ca uptake sarcoplasmic reticulum Ca2+ free ATP MgATP 

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References

  1. 1.
    Brandt, P.W., Cox, R.N., Kawai, M. 1980. Can the binding of Ca2+ to the regulatory sites on troponin-C determine the steep pCa/tension relationship of skeletal muscle?Proc. Natl. Acad. Sci. USA 77:4717–4720PubMedGoogle Scholar
  2. 2.
    Briggs, F.N., Poland, J.L., Solaro, R.J. 1977. Relative capabilities of sarcoplasmic reticulum in fast and slow mammalian skeletal muscles.J. Physiol. (London) 266:587–594Google Scholar
  3. 3.
    Chapman, R.A., Miller, D.J. 1974. Structure-activity relations for caffeine: A comparative study of the inotropic effects of the methylxanthines, imidazoles and related compounds on the frog's heart.J. Physiol. (London) 242:615–634Google Scholar
  4. 4.
    Chiarandini, D.J., Reuben, J.P., Brandt, P.W., Grundfest, H. 1970. Effects of caffeine on crayfish muscle fibers. I. Activation of contraction and induction of Ca spike electrogenesis.J. Gen. Physiol. 55:640–664Google Scholar
  5. 5.
    Chiarandini, D.J., Reuben, J.P., Girardier, L., Katz, G.M., Grundfest, H. 1970. Effects of caffeine on crayfish muscle fibers. II. Refractoriness and factors influencing recovery (repriming) of contractile responses.J. Gen. Physiol. 55:665–687Google Scholar
  6. 6.
    Chiesi, M., Wen, Y.S. 1983. A phosphorylated conformational state of the (Ca2+−Mg2+)-ATPase of fast skeletal muscle sarcoplasmic reticulum can mediate rapid Ca2+ release.J. Biol. Chem. 258:6078–6085PubMedGoogle Scholar
  7. 7.
    De Meis, L., Hasselbach, W. 1971. Acetylphosphate as substrate for Ca2+ uptake in skeletal muscle microsomes.J. Biol. Chem. 246:4759–4763Google Scholar
  8. 8.
    De Meis, L., Vianna, A.L. 1979. Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum.Annu. Rev. Biochem. 48:275–292PubMedGoogle Scholar
  9. 9.
    Eastwood, A.B., Wood, D.S., Bock, K.L., Sorenson, M.M. 1979. Chemically skinned mammalian skeletal muscle. I. The structure of skinned rabbit psoas.Tissue Cell 11:553–566PubMedGoogle Scholar
  10. 10.
    Endo, M. 1975. Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle.Proc. Jpn. Acad. 51:479–484Google Scholar
  11. 11.
    Endo, M., Kitazawa, T. 1976. The effect of ATP on calcium release mechanisms in the sarcoplasmic reticulum of skinned muscle fibers.Proc. Jpn. Acad. 52:595–598Google Scholar
  12. 12.
    Endo, M., Tanaka, M., Ogawa, Y. 1970. Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres.Nature (London) 228:34–36Google Scholar
  13. 13.
    Fabiato, A., Fabiato, F. 1979. Calculator programs for computing the concentrations of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells.J. Physiol. (Paris) 75:463–505Google Scholar
  14. 14.
    Fairhurst, A.S. 1974. A ryanodine-caffeine sensitive membrane fraction of skeletal muscle.Am. J. Physiol. 227:1124–1131PubMedGoogle Scholar
  15. 15.
    Fairhurst, A.S., Hasselbach, W. 1970. Calcium efflux from a heavy sarcotubular fraction: Effects of ryanodine, caffeine and magnesium.Eur. J. Biochem. 13:504–509PubMedGoogle Scholar
  16. 16.
    Feher, J.J., Briggs, N. 1980. The effect of calcium oxalate crystallization kinetics on the kinetics of calcium uptake and calcium ATPase activity of sarcoplasmic reticulum vesicles.Cell Calcium 1:105–118Google Scholar
  17. 17.
    Frank, G.B. 1962. Utilization of bound calcium in the action of caffeine and certain multivalent cations on skeletal muscle.J. Physiol. (London) 163:254–268Google Scholar
  18. 18.
    Fuchs, F. 1969. Inhibition of sarcotubular calcium transport by caffeine: Species and temperature dependence.Biochim. Biophys. Acta 172:566–570PubMedGoogle Scholar
  19. 19.
    Hasselbach, W. 1966. Structural and enzymatic properties of the calcium transporting membranes of the sarcoplasmic reticulum.Ann. N.Y. Acad. Sci. 137:1041–1048PubMedGoogle Scholar
  20. 20.
    Johnson, P.N., Inesi, G. 1969. The effect of methylxanthines and local anesthetics on fragmented sarcoplasmic reticulum.J. Pharmacol. Exp. Ther. 169:308–314PubMedGoogle Scholar
  21. 21.
    Katz, A.M., Repke, D.I., 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. 252:1938–1949PubMedGoogle Scholar
  22. 22.
    Kim, D.H., Ohnishi, S.T., Ikemoto, N. 1983. Kinetic studies of calcium release from sarcoplasmic reticulumin vitro.J. Biol. Chem. 258:9662–9668PubMedGoogle Scholar
  23. 23.
    Kirino, Y., Osakabe, M., Shimizu, H. 1983. Ca2+-induced Ca2+ release from fragmented sarcoplasmic reticulum: Ca2+-dependent passive Ca2+ efflux.J. Biochem. 94:1111–1118PubMedGoogle Scholar
  24. 24.
    Kirino, Y., Shimizu, H. 1982. Ca2+-induced Ca2+ release from fragmented sarcoplasmic reticulum: A comparison with skinned muscle fiber studies.J. Biochem. 92:1287–1296PubMedGoogle Scholar
  25. 25.
    Kitazawa, T., Endo, M. 1976. Increase in passive calcium influx into the sarcoplasmic reticulum by “depolarization” and caffeine.Proc. Jpn. Acad. 52:599–602Google Scholar
  26. 26.
    Koeppe, P., Hamann, C. 1980. A program for non-linear regression analysis to be used on desk-top computers.Comput. Prog. Biomed. 12:121–128Google Scholar
  27. 27.
    Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. 1951. Protein measurement with the Folin phenol reagent.J. Biol. Chem. 193:265–275PubMedGoogle Scholar
  28. 28.
    Lüttgau, H.C., Oetliker, H. 1968. The action of caffeine on the activation of the contractile mechanism in striated muscle fibers.J. Physiol. (London) 194:51–74Google Scholar
  29. 29.
    Meissner, G. 1975. Isolation and characterization of two types of sarcoplasmic reticulum vesicles.Biochim. Biophys. Acta 389:51–68PubMedGoogle Scholar
  30. 30.
    Meissner, G. 1984. Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum.J. Biol. Chem. 259:2365–2374PubMedGoogle Scholar
  31. 31.
    Meissner, G., Conner, G.E., Fleischer, S. 1973. Isolation of sarcoplasmic reticulum by zonal centrifugation and purification of Ca2+-pump protein and Ca2+-binding proteins.Biochim. Biophys. Acta 298:246–269PubMedGoogle Scholar
  32. 32.
    Miledi, R., Stefani, E. 1969. Non-selective re-innervation of slow and fast muscle fibres in the rat.Nature (London) 222:569–571Google Scholar
  33. 33.
    Millman, M., Azari, J. 1977. Adenosine-triphosphate-induced rapid calcium release from fragmented sarcoplasmic reticulum.Biochem. Biophys. Res. Commun. 78:60–66PubMedGoogle Scholar
  34. 34.
    Miyamoto, H., Racker, E. 1982. Mechanism of calcium release from skeletal sarcoplasmic reticulum.J. Membrane Biol. 66:193–201Google Scholar
  35. 35.
    Nagasaki, K., Kasai, M. 1981. Calcium-induced calcium release from sarcoplasmic reticulum vesicles.J. Biochem. 90:749–755PubMedGoogle Scholar
  36. 36.
    Nagasaki, K., Kasai, M. 1983. Fast release of calcium from sarcoplasmic reticulum vesicles monitored by chlortetracycline fluorescence.J. Biochem. 94:1104–1109Google Scholar
  37. 37.
    Ogawa, Y. 1970. Some properties of fragmented frog sarcoplasmic reticulum with particular reference to its response to caffeine.J. Biochem. 67:667–683PubMedGoogle Scholar
  38. 38.
    Ogawa, Y., Ebashi, S. 1973. Ca2+ uptake and release by fragmented sarcoplasmic reticulum with special reference to the effect of β,γ-methylene adenosine triphosphate.In: Organization of Energy-transducing Membranes. M. Nakao and L. Packer, editors. pp. 127–140. University Park Press, TokyoGoogle Scholar
  39. 39.
    Ohnishi, S.T. 1979. Calcium-induced calcium release from fragmented sarcoplasmic reticulum.J. Biochem. 86:1147–1150PubMedGoogle Scholar
  40. 40.
    Solaro, R.J., Briggs, F.N. 1974. Estimating the functional capabilities of sarcoplasmic reticulum in cardiac muscle.Circ. Res. 34:531–540PubMedGoogle Scholar
  41. 41.
    Somlyo, A.V., Gonzales-Serratos, H., Shuman, H., McClellan, G., Somlyo, A.P. 1982. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: An electron-probe study.J. Cell Biol. 90:577–594Google Scholar
  42. 42.
    Sorenson, M., Coelho, H.S.L. 1984. Caffeine inhibition of calcium accumulation by the sarcoplasmic reticulum in mammalian skeletal muscle fibers.Braz. J. Med. Biol. Res. 17:398Google Scholar
  43. 43.
    Sorenson, M., Coelho, H.S.L. 1985. Caffeine inhibition of Ca++ accumulation in skinned fibers.Biophys. J. 47:452aGoogle Scholar
  44. 44.
    Sorenson, M., Eastwood, A.B., Reuben, J.P. 1978. Caffeine sensitivity of the sarcoplasmic reticulum: Heterogeneous distribution within sarcomeres of skinned fibers.VIth Intl. Congr. Biophys., Kyoto, p. 234Google Scholar
  45. 45.
    Sorenson, M.M., Reuben, J.P., Eastwood, A.B., Orentlicher, M., Katz, G.M. 1980. Functional heterogeneity of the sarcoplasmic reticulum within sarcomeres of skinned muscle fibers.J. Membrane Biol. 53:1–17Google Scholar
  46. 46.
    Stephenson, E.W. 1981. Ca2+ dependence of stimulated45Ca efflux in skinned muscle fibers.J. Gen. Physiol. 77:419–443PubMedGoogle Scholar
  47. 47.
    Su, J.Y., Hasselbach, W. 1984. Caffeine-induced calcium release from isolated sarcoplasmic reticulum of rabbit skeletal muscle.Pfluegers Arch. 400:14–21Google Scholar
  48. 48.
    Verjovski-Almeida, S., Inesi, G. 1979. Fast-kinetic evidence for an activating effect of ATP on the Ca2+ transport of sarcoplasmic reticulum ATPase.J. Biol. Chem. 254:18–21Google Scholar
  49. 49.
    Vianna, A.L. 1975. Interaction of calcium and magnesium in activating and inhibiting the nucleoside triphosphatase of sarcoplasmic reticulum vesicles.Biochim. Biophys. Acta 410:389–406Google Scholar
  50. 50.
    Volpe, P., Mrak, R.E., Costello, B., Fleischer, S. 1984. Calcium release from sarcoplasmic reticulum of normal and dystrophic mice.Biochim. Biophys. Acta 769:67–78PubMedGoogle Scholar
  51. 51.
    Weber, A. 1968. The mechanism of action of caffeine on sarcoplasmic reticulum.J. Gen. Physiol. 52:760–772PubMedGoogle Scholar
  52. 52.
    Weber, A., Herz, R. 1968. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum.J. Gen. Physiol. 52:750–759Google Scholar
  53. 53.
    Winegrad, S. 1968. Intracellular calcium movements of frog skeletal muscle during recovery from a tetanus.J. Gen. Physiol. 51:65–83PubMedGoogle Scholar
  54. 54.
    Wood, D.S. 1978. Human skeletal muscle: Analysis of Ca2+ regulation in skinned fibers using caffeine.Exp. Neurol. 58:218–230PubMedGoogle Scholar
  55. 55.
    Wood, D.S., Kahn, D.A., Selinger, S., Reuben, J.P. 1977. Regulation of Ca++ efflux from the SR by ATP, Mg++ and Pi in the absence of substrate in skinned mammalian skeletal muscle.Biophys. J. 17:201Google Scholar
  56. 56.
    Wood, D.S., Zollman, J., Reuben, J.P., Brandt, P.W. 1975. Human skeletal muscle: Properties of the “chemically skinned” fiber.Science 187:1075–1076Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1986

Authors and Affiliations

  • M. M. Sorenson
    • 1
  • H. S. L. Coelho
    • 1
  • J. P. Reuben
    • 1
  1. 1.Departamento de Bioquímica, ICB, Universidade Federal do Rio de JaneiroCidade UniversitáriaRio de JaneiroBrasil

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