Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1989 Sep;416:435–454. doi: 10.1113/jphysiol.1989.sp017770

Actions of caffeine on fast- and slow-twitch muscles of the rat.

M W Fryer 1, I R Neering 1
PMCID: PMC1189224  PMID: 2607458

Abstract

1. The effects of caffeine (0.2-20 mmol l-1) have been examined on calcium transients (measured with aequorin) and isometric force in intact bundles of fibres from soleus (slow-twitch) and extensor digitorum longus (EDL; fast-twitch) muscles of the rat. 2. At 25 degrees C, threshold caffeine concentration for an observable increase in resting [Ca2+]i was 0.2 and 1.0 mmol l-1 for soleus and EDL muscles respectively. Increases in resting force were first detectable at about 0.5 mmol l-1 caffeine for soleus muscles and 5.0 mmol l-1 caffeine for EDL muscles and occurred in the range 0.2-0.4 mumol l-1 [Ca2+]i for soleus and 0.7-0.9 mumol l-1 for EDL. 3. Caffeine potentiated the twitch responses of soleus and EDL in a dose-related manner. The soleus was more sensitive in this respect, with 50% potentiation occurring at 1 mmol l-1 caffeine compared with 3.5 mmol l-1 for the EDL. Concentrations of caffeine below 2 mmol l-1 potentiated Ca2+ transients associated with twitches in both soleus and EDL muscles with no apparent change in the decay rate constant. 4. High concentrations of caffeine (greater than 2 mmol l-1) further potentiated peak Ca2+ in the EDL but depressed it in the soleus. The rate of decay of the Ca2+ transient in high caffeine was significantly prolonged in the soleus but remained unaffected in the EDL. 5. The phosphodiesterase inhibitor, 3-isobutyl-1-methylxanthine (IBMX) had little effect on force or [Ca2+]i at concentrations known to significantly increase intracellular cyclic AMP levels. 6. The Ca2+ transient during fused tetani was characterized by an initial peak, a decline to a plateau level and sometimes a gradual rise towards the end of the stimulus train. Peak [Ca2+]i during normal tetani ranged between 1.1 and 2.4 mumol l-1 in the soleus and 1.9 and 4.0 mumol l-1 in the EDL. 7. Caffeine potentiated both force and [Ca2+]i during tetanus. Since the increase of the Ca2+ transient was significantly greater than potentiation of force, it is likely that saturation of myofilaments occurs. The primary effect of caffeine on the Ca2+ transient was an elevation of the plateau phase. 8. Caffeine concentrations below 5 mmol l-1 potentiate twitch and tetanic force in both fast- and slow-twitch mammalian skeletal muscles primarily by increasing both the basal and stimulus-evoked release of Ca2+ from the sarcoplasmic reticulum.

Full text

PDF
438

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AXELSSON J., THESLEFF S. Activation of the contractile mechanism in striated muscle. Acta Physiol Scand. 1958 Oct 28;44(1):55–66. doi: 10.1111/j.1748-1716.1958.tb01608.x. [DOI] [PubMed] [Google Scholar]
  2. Abercrombie R. F., Roos A. The intracellular pH of frog skeletal muscle: its regulation in hypertonic solutions. J Physiol. 1983 Dec;345:189–204. doi: 10.1113/jphysiol.1983.sp014974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allen D. G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982 Jun;327:79–94. doi: 10.1113/jphysiol.1982.sp014221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blinks J. R., Rüdel R., Taylor S. R. Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin. J Physiol. 1978 Apr;277:291–323. doi: 10.1113/jphysiol.1978.sp012273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blinks J. R., Wier W. G., Hess P., Prendergast F. G. Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol. 1982;40(1-2):1–114. doi: 10.1016/0079-6107(82)90011-6. [DOI] [PubMed] [Google Scholar]
  6. Cannell M. B., Allen D. G. Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys J. 1984 May;45(5):913–925. doi: 10.1016/S0006-3495(84)84238-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Celio M. R., Heizmann C. W. Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature. 1982 Jun 10;297(5866):504–506. doi: 10.1038/297504a0. [DOI] [PubMed] [Google Scholar]
  8. Connett R. J., Ugol L. M., Hammack M. J., Hays E. T. Twitch potentiation and caffeine contractures in isolated rat soleus muscle. Comp Biochem Physiol C. 1983;74(2):349–354. doi: 10.1016/0742-8413(83)90113-5. [DOI] [PubMed] [Google Scholar]
  9. Delay M., Ribalet B., Vergara J. Caffeine potentiation of calcium release in frog skeletal muscle fibres. J Physiol. 1986 Jun;375:535–559. doi: 10.1113/jphysiol.1986.sp016132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dulhunty A. F., Banyard M. R., Medveczky C. J. Distribution of calcium ATPase in the sarcoplasmic reticulum of fast- and slow-twitch muscles determined with monoclonal antibodies. J Membr Biol. 1987;99(2):79–92. doi: 10.1007/BF01871228. [DOI] [PubMed] [Google Scholar]
  11. Duncan C. J., Smith J. L. The action of caffeine in promoting ultrastructural damage in frog skeletal muscle fibres. Evidence for the involvement of the calcium-induced release of calcium from the sarcoplasmic reticulum. Naunyn Schmiedebergs Arch Pharmacol. 1978 Nov;305(2):159–166. doi: 10.1007/BF00508287. [DOI] [PubMed] [Google Scholar]
  12. Eusebi F., Miledi R., Takahashi T. Calcium transients in mammalian muscles. Nature. 1980 Apr 10;284(5756):560–561. doi: 10.1038/284560a0. [DOI] [PubMed] [Google Scholar]
  13. Fairhurst A. S. A ryanodine-caffeine-sensitive membrane fraction of skeletal muscle. Am J Physiol. 1974 Nov;227(5):1124–1131. doi: 10.1152/ajplegacy.1974.227.5.1124. [DOI] [PubMed] [Google Scholar]
  14. Fryer M. W., Neering I. R. Relationship between intracellular calcium concentration and relaxation of rat fast and slow muscles. Neurosci Lett. 1986 Feb 28;64(2):231–235. doi: 10.1016/0304-3940(86)90106-0. [DOI] [PubMed] [Google Scholar]
  15. Fryer M. W., Neering I. R., Stephenson D. G. Effects of 2,3-butanedione monoxime on the contractile activation properties of fast- and slow-twitch rat muscle fibres. J Physiol. 1988 Dec;407:53–75. doi: 10.1113/jphysiol.1988.sp017403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fuchs F. Inhibition of sarcotubular calcium transport by caffeine: species and temperature dependence. Biochim Biophys Acta. 1969 Apr 8;172(3):566–570. doi: 10.1016/0005-2728(69)90152-2. [DOI] [PubMed] [Google Scholar]
  17. Iaizzo P. A., Klein W., Lehmann-Horn F. Fura-2 detected myoplasmic calcium and its correlation with contracture force in skeletal muscle from normal and malignant hyperthermia susceptible pigs. Pflugers Arch. 1988 Jun;411(6):648–653. doi: 10.1007/BF00580861. [DOI] [PubMed] [Google Scholar]
  18. Isaacson A., Hinkes M. J., Taylor S. R. Contracture and twitch potentiation of fast and slow muscles of the rat at 20 and 37 C. Am J Physiol. 1970 Jan;218(1):33–41. doi: 10.1152/ajplegacy.1970.218.1.33. [DOI] [PubMed] [Google Scholar]
  19. Konishi M., Kurihara S. Effects of caffeine on intracellular calcium concentrations in frog skeletal muscle fibres. J Physiol. 1987 Feb;383:269–283. doi: 10.1113/jphysiol.1987.sp016408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Konishi M., Kurihara S., Sakai T. Change in intracellular calcium ion concentration induced by caffeine and rapid cooling in frog skeletal muscle fibres. J Physiol. 1985 Aug;365:131–146. doi: 10.1113/jphysiol.1985.sp015763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kovács L., Szücs G. Effect of caffeine on intramembrane charge movement and calcium transients in cut skeletal muscle fibres of the frog. J Physiol. 1983 Aug;341:559–578. doi: 10.1113/jphysiol.1983.sp014824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kramer G. L., Wells J. N. Xanthines and skeletal muscle: lack of relationship between phosphodiesterase inhibition and increased twitch tension in rat diaphragms. Mol Pharmacol. 1980 Jan;17(1):73–78. [PubMed] [Google Scholar]
  23. Leberer E., Pette D. Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles of defined fiber composition. Eur J Biochem. 1986 May 2;156(3):489–496. doi: 10.1111/j.1432-1033.1986.tb09607.x. [DOI] [PubMed] [Google Scholar]
  24. Lopez J. R., Wanek L. A., Taylor S. R. Skeletal muscle: length-dependent effects of potentiating agents. Science. 1981 Oct 2;214(4516):79–82. doi: 10.1126/science.6974399. [DOI] [PubMed] [Google Scholar]
  25. Lüttgau H. C., Oetliker H. The action of caffeine on the activation of the contractile mechanism in straited muscle fibres. J Physiol. 1968 Jan;194(1):51–74. doi: 10.1113/jphysiol.1968.sp008394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McBurney R. N., Neering I. R. The measurement of changes in intracellular free calcium during action potentials in mammalian neurones. J Neurosci Methods. 1985 Mar;13(1):65–76. doi: 10.1016/0165-0270(85)90044-5. [DOI] [PubMed] [Google Scholar]
  27. Miledi R., Parker I., Zhu P. H. Calcium transients evoked by action potentials in frog twitch muscle fibres. J Physiol. 1982 Dec;333:655–679. doi: 10.1113/jphysiol.1982.sp014474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Morgan J. P., Blinks J. R. Intracellular Ca2+ transients in the cat papillary muscle. Can J Physiol Pharmacol. 1982 Apr;60(4):524–528. doi: 10.1139/y82-072. [DOI] [PubMed] [Google Scholar]
  29. Pagala M. K. Effect of length and caffeine on isometric tetanus relaxation of frog sartorius muscles. Biochim Biophys Acta. 1980 Jun 10;591(1):177–186. doi: 10.1016/0005-2728(80)90231-5. [DOI] [PubMed] [Google Scholar]
  30. SANDOW A., TAYLOR S. R., ISAASON A., SEGUIN J. J. ELECTROCHEMICAL COUPLING IN POTENTIATION OF MUSCULAR CONTRACTION. Science. 1964 Feb 7;143(3606):577–579. doi: 10.1126/science.143.3606.577. [DOI] [PubMed] [Google Scholar]
  31. Sorenson M. M., Coelho H. S., Reuben J. P. Caffeine inhibition of calcium accumulation by the sarcoplasmic reticulum in mammalian skinned fibers. J Membr Biol. 1986;90(3):219–230. doi: 10.1007/BF01870128. [DOI] [PubMed] [Google Scholar]
  32. Stephenson D. G., Williams D. A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J Physiol. 1981 Aug;317:281–302. doi: 10.1113/jphysiol.1981.sp013825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stephenson E. W. Ca2+ dependence of stimulated 45Ca efflux in skinned muscle fibers. J Gen Physiol. 1981 Apr;77(4):419–443. doi: 10.1085/jgp.77.4.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Su J. Y., Hasselbach W. Caffeine-induced calcium release from isolated sarcoplasmic reticulum of rabbit skeletal muscle. Pflugers Arch. 1984 Jan;400(1):14–21. doi: 10.1007/BF00670530. [DOI] [PubMed] [Google Scholar]
  35. Weber A., Herz R. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol. 1968 Nov;52(5):750–759. doi: 10.1085/jgp.52.5.750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wendt I. R., Stephenson D. G. Effects of caffeine on Ca-activated force production in skinned cardiac and skeletal muscle fibres of the rat. Pflugers Arch. 1983 Aug;398(3):210–216. doi: 10.1007/BF00657153. [DOI] [PubMed] [Google Scholar]
  37. Yoshioka T., Somlyo A. P. Calcium and magnesium contents and volume of the terminal cisternae in caffeine-treated skeletal muscle. J Cell Biol. 1984 Aug;99(2):558–568. doi: 10.1083/jcb.99.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES