Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1995 Mar 1;105(3):363–383. doi: 10.1085/jgp.105.3.363

T-tubule depolarization-induced SR Ca2+ release is controlled by dihydropyridine receptor- and Ca(2+)-dependent mechanisms in cell homogenates from rabbit skeletal muscle

PMCID: PMC2216947  PMID: 7769380

Abstract

In vertebrate skeletal muscle, the voltage-dependent mechanism of rapid sarcoplasmic reticulum (SR) Ca2+ release, commonly referred to as excitation-contraction (EC) coupling, is believed to be mediated by physical interaction between the transverse (T)-tubule voltage-sensing dihydropyridine receptor (DHPR) and the SR ryanodine receptor (RyR)/Ca2+ release channel. In this study, differential T-tubule and SR membrane monovalent ion permeabilities were exploited with the use of an ion-replacement protocol to study T-tubule depolarization-induced SR 45Ca2+ release from rabbit skeletal muscle whole-cell homogenates. Specificity of Ca2+ release was ascertained with the use of the DHPR antagonists D888, nifedipine and PN200-110. In the presence of the "slow" complexing Ca2+ buffer EGTA, homogenates exhibited T-tubule depolarization-induced Ca2+ release comprised of an initial rapid phase followed by a slower release phase. During the rapid phase, approximately 20% of the total sequestered Ca2+ (approximately 30 nmol 45Ca2+/mg protein), corresponding to 100% of the caffeine-sensitive Ca2+ pool, was released within 50 ms. Rapid release could be inhibited fourfold by D888. Addition to release media of the "fast" complexing Ca2+ buffer BAPTA, at concentrations > or = 4 mM, nearly abolished rapid Ca2+ release, suggesting that most was Ca2+ dependent. Addition of millimolar concentrations of either Ca2+ or Mg2+ also greatly reduced rapid Ca2+ release. These results show that T-tubule depolarization-induced SR Ca2+ release from rabbit skeletal muscle homogenates is controlled by T-tubule membrane potential- and by Ca(2+)- dependent mechanisms.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Anderson K., Cohn A. H., Meissner G. High-affinity [3H]PN200-110 and [3H]ryanodine binding to rabbit and frog skeletal muscle. Am J Physiol. 1994 Feb;266(2 Pt 1):C462–C466. doi: 10.1152/ajpcell.1994.266.2.C462. [DOI] [PubMed] [Google Scholar]
  2. Armstrong C. M., Bezanilla F. M., Horowicz P. Twitches in the presence of ethylene glycol bis( -aminoethyl ether)-N,N'-tetracetic acid. Biochim Biophys Acta. 1972 Jun 23;267(3):605–608. doi: 10.1016/0005-2728(72)90194-6. [DOI] [PubMed] [Google Scholar]
  3. Baylor S. M., Chandler W. K., Marshall M. W. Optical measurements of intracellular pH and magnesium in frog skeletal muscle fibres. J Physiol. 1982 Oct;331:105–137. doi: 10.1113/jphysiol.1982.sp014367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor S. M., Chandler W. K., Marshall M. W. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol. 1983 Nov;344:625–666. doi: 10.1113/jphysiol.1983.sp014959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beuckelmann D. J., Wier W. G. Mechanism of release of calcium from sarcoplasmic reticulum of guinea-pig cardiac cells. J Physiol. 1988 Nov;405:233–255. doi: 10.1113/jphysiol.1988.sp017331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Block B. A., Imagawa T., Campbell K. P., Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol. 1988 Dec;107(6 Pt 2):2587–2600. doi: 10.1083/jcb.107.6.2587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brandt N. R., Caswell A. H., Brunschwig J. P., Kang J. J., Antoniu B., Ikemoto N. Effects of anti-triadin antibody on Ca2+ release from sarcoplasmic reticulum. FEBS Lett. 1992 Mar 24;299(1):57–59. doi: 10.1016/0014-5793(92)80100-u. [DOI] [PubMed] [Google Scholar]
  8. Brum G., Stefani E., Rios E. Simultaneous measurements of Ca2+ currents and intracellular Ca2+ concentrations in single skeletal muscle fibers of the frog. Can J Physiol Pharmacol. 1987 Apr;65(4):681–685. doi: 10.1139/y87-112. [DOI] [PubMed] [Google Scholar]
  9. Corbett A. M., Bian J., Wade J. B., Schneider M. F. Depolarization-induced calcium release from isolated triads measured with impermeant fura-2. J Membr Biol. 1992 Jun;128(3):165–179. doi: 10.1007/BF00231810. [DOI] [PubMed] [Google Scholar]
  10. Csernoch L., Jacquemond V., Schneider M. F. Microinjection of strong calcium buffers suppresses the peak of calcium release during depolarization in frog skeletal muscle fibers. J Gen Physiol. 1993 Feb;101(2):297–333. doi: 10.1085/jgp.101.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dunn S. M. Voltage-dependent calcium channels in skeletal muscle transverse tubules. Measurements of calcium efflux in membrane vesicles. J Biol Chem. 1989 Jul 5;264(19):11053–11060. [PubMed] [Google Scholar]
  12. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  13. Erdmann R., Lüttgau H. C. The effect of the phenylalkylamine D888 (devapamil) on force and Ca2+ current in isolated frog skeletal muscle fibres. J Physiol. 1989 Jun;413:521–541. doi: 10.1113/jphysiol.1989.sp017667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):247–289. doi: 10.1085/jgp.85.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Feldmeyer D., Melzer W., Pohl B. Effects of gallopamil on calcium release and intramembrane charge movements in frog skeletal muscle fibres. J Physiol. 1990 Feb;421:343–362. doi: 10.1113/jphysiol.1990.sp017948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Franzini-Armstrong C., Jorgensen A. O. Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol. 1994;56:509–534. doi: 10.1146/annurev.ph.56.030194.002453. [DOI] [PubMed] [Google Scholar]
  17. Gupta R. K., Moore R. D. 31P NMR studies of intracellular free Mg2+ in intact frog skeletal muscle. J Biol Chem. 1980 May 10;255(9):3987–3993. [PubMed] [Google Scholar]
  18. Hollingworth S., Harkins A. B., Kurebayashi N., Konishi M., Baylor S. M. Excitation-contraction coupling in intact frog skeletal muscle fibers injected with mmolar concentrations of fura-2. Biophys J. 1992 Jul;63(1):224–234. doi: 10.1016/S0006-3495(92)81599-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ikemoto N., Antoniu B., Kang J. J. Characterization of "depolarization"-induced calcium release from sarcoplasmic reticulum in vitro with the use of membrane potential probe. Biochem Biophys Res Commun. 1992 Apr 15;184(1):538–543. doi: 10.1016/0006-291x(92)91228-i. [DOI] [PubMed] [Google Scholar]
  20. Ikemoto N., Antoniu B., Mészáros L. G. Rapid flow chemical quench studies of calcium release from isolated sarcoplasmic reticulum. J Biol Chem. 1985 Nov 15;260(26):14096–14100. [PubMed] [Google Scholar]
  21. Jacquemond V., Csernoch L., Klein M. G., Schneider M. F. Voltage-gated and calcium-gated calcium release during depolarization of skeletal muscle fibers. Biophys J. 1991 Oct;60(4):867–873. doi: 10.1016/S0006-3495(91)82120-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jong D. S., Pape P. C., Chandler W. K., Baylor S. M. Reduction of calcium inactivation of sarcoplasmic reticulum calcium release by fura-2 in voltage-clamped cut twitch fibers from frog muscle. J Gen Physiol. 1993 Aug;102(2):333–370. doi: 10.1085/jgp.102.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lai F. A., Liu Q. Y., Xu L., el-Hashem A., Kramarcy N. R., Sealock R., Meissner G. Amphibian ryanodine receptor isoforms are related to those of mammalian skeletal or cardiac muscle. Am J Physiol. 1992 Aug;263(2 Pt 1):C365–C372. doi: 10.1152/ajpcell.1992.263.2.C365. [DOI] [PubMed] [Google Scholar]
  24. Lamb G. D., Stephenson D. G. Control of calcium release and the effect of ryanodine in skinned muscle fibres of the toad. J Physiol. 1990 Apr;423:519–542. doi: 10.1113/jphysiol.1990.sp018037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lamb G. D., Stephenson D. G. Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. J Physiol. 1991 Mar;434:507–528. doi: 10.1113/jphysiol.1991.sp018483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lu X., Xu L., Meissner G. Activation of the skeletal muscle calcium release channel by a cytoplasmic loop of the dihydropyridine receptor. J Biol Chem. 1994 Mar 4;269(9):6511–6516. [PubMed] [Google Scholar]
  27. Meissner G. Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum. J Biol Chem. 1984 Feb 25;259(4):2365–2374. [PubMed] [Google Scholar]
  28. Meissner G. Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum. Mol Cell Biochem. 1983;55(1):65–82. doi: 10.1007/BF00229243. [DOI] [PubMed] [Google Scholar]
  29. Meissner G. Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol. 1994;56:485–508. doi: 10.1146/annurev.ph.56.030194.002413. [DOI] [PubMed] [Google Scholar]
  30. Melzer W., Rios E., Schneider M. F. Time course of calcium release and removal in skeletal muscle fibers. Biophys J. 1984 Mar;45(3):637–641. doi: 10.1016/S0006-3495(84)84203-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Miledi R., Parker I., Zhu P. H. Extracellular ions and excitation-contraction coupling in frog twitch muscle fibres. J Physiol. 1984 Jun;351:687–710. doi: 10.1113/jphysiol.1984.sp015271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Murayama T., Ogawa Y. Purification and characterization of two ryanodine-binding protein isoforms from sarcoplasmic reticulum of bullfrog skeletal muscle. J Biochem. 1992 Oct;112(4):514–522. doi: 10.1093/oxfordjournals.jbchem.a123931. [DOI] [PubMed] [Google Scholar]
  33. Olivares E. B., Tanksley S. J., Airey J. A., Beck C. F., Ouyang Y., Deerinck T. J., Ellisman M. H., Sutko J. L. Nonmammalian vertebrate skeletal muscles express two triad junctional foot protein isoforms. Biophys J. 1991 Jun;59(6):1153–1163. doi: 10.1016/S0006-3495(91)82331-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pape P. C., Jong D. S., Chandler W. K., Baylor S. M. Effect of fura-2 on action potential-stimulated calcium release in cut twitch fibers from frog muscle. J Gen Physiol. 1993 Aug;102(2):295–332. doi: 10.1085/jgp.102.2.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Richardson A., Taylor C. W. Effects of Ca2+ chelators on purified inositol 1,4,5-trisphosphate (InsP3) receptors and InsP3-stimulated Ca2+ mobilization. J Biol Chem. 1993 Jun 5;268(16):11528–11533. [PubMed] [Google Scholar]
  36. Rousseau E., Ladine J., Liu Q. Y., Meissner G. Activation of the Ca2+ release channel of skeletal muscle sarcoplasmic reticulum by caffeine and related compounds. Arch Biochem Biophys. 1988 Nov 15;267(1):75–86. doi: 10.1016/0003-9861(88)90010-0. [DOI] [PubMed] [Google Scholar]
  37. Ríos E., Pizarro G. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev. 1991 Jul;71(3):849–908. doi: 10.1152/physrev.1991.71.3.849. [DOI] [PubMed] [Google Scholar]
  38. Sabbadini R. A., Dahms A. S. Biochemical properties of isolated transverse tubular membranes. J Bioenerg Biomembr. 1989 Apr;21(2):163–213. doi: 10.1007/BF00812068. [DOI] [PubMed] [Google Scholar]
  39. Schneider M. F. Control of calcium release in functioning skeletal muscle fibers. Annu Rev Physiol. 1994;56:463–484. doi: 10.1146/annurev.ph.56.030194.002335. [DOI] [PubMed] [Google Scholar]
  40. Schoenmakers T. J., Visser G. J., Flik G., Theuvenet A. P. CHELATOR: an improved method for computing metal ion concentrations in physiological solutions. Biotechniques. 1992 Jun;12(6):870-4, 876-9. [PubMed] [Google Scholar]
  41. Simon B. J., Klein M. G., Schneider M. F. Calcium dependence of inactivation of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. J Gen Physiol. 1991 Mar;97(3):437–471. doi: 10.1085/jgp.97.3.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stephenson E. W. Excitation of skinned muscle fibers by imposed ion gradients. I. Stimulation of 45Ca efflux at constant [K][Cl] product. J Gen Physiol. 1985 Dec;86(6):813–832. doi: 10.1085/jgp.86.6.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stephenson E. W., Podolsky R. J. Influence of magnesium on chloride-induced calcium release in skinned muscle fibers. J Gen Physiol. 1977 Jan;69(1):17–35. doi: 10.1085/jgp.69.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stern M. D. Buffering of calcium in the vicinity of a channel pore. Cell Calcium. 1992 Mar;13(3):183–192. doi: 10.1016/0143-4160(92)90046-u. [DOI] [PubMed] [Google Scholar]
  45. Volpe P., Stephenson E. W. Ca2+ dependence of transverse tubule-mediated calcium release in skinned skeletal muscle fibers. J Gen Physiol. 1986 Feb;87(2):271–288. doi: 10.1085/jgp.87.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wagenknecht T., Grassucci R., Frank J., Saito A., Inui M., Fleischer S. Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature. 1989 Mar 9;338(6211):167–170. doi: 10.1038/338167a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES