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. 2002 Mar;82(3):1509–1523. doi: 10.1016/S0006-3495(02)75504-5

Sustained release of calcium elicited by membrane depolarization in ryanodine-injected mouse skeletal muscle fibers.

Claude Collet 1, Vincent Jacquemond 1
PMCID: PMC1301951  PMID: 11867465

Abstract

The effect of micromolar intracellular levels of ryanodine was tested on the myoplasmic free calcium concentration ([Ca(2+)](i)) measured from a portion of isolated mouse skeletal muscle fibers voltage-clamped at -80 mV. When ryanodine-injected fibers were transiently depolarized to 0 mV, the early decay phase of [Ca(2+)](i) upon membrane repolarization was followed by a steady elevated [Ca(2+)](i) level. This effect could be qualitatively well simulated, assuming that ryanodine binds to release channels that open during depolarization and that ryanodine-bound channels do not close upon repolarization. The amplitude of the postpulse [Ca(2+)](i) elevation depended on the duration of the depolarization, being hardly detectable for pulses shorter than 100 ms, and very prominent for duration pulses of seconds. Within a series of consecutive pulses of the same duration, the effect of ryanodine produced a staircase increase in resting [Ca(2+)](i), the slope of which was approximately twice larger for depolarizations to 0 or +10 mV than to -30 or -20 mV. Overall results are consistent with the "open-locked" state because of ryanodine binding to calcium release channels that open during depolarization. Within the voltage-sensitive range of calcium release, increasing either the amplitude or the duration of the depolarization seems to enhance the fraction of release channels accessible to ryanodine.

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Selected References

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  1. 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]
  2. Brum G., Ríos E., Stéfani E. Effects of extracellular calcium on calcium movements of excitation-contraction coupling in frog skeletal muscle fibres. J Physiol. 1988 Apr;398:441–473. doi: 10.1113/jphysiol.1988.sp017052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buck E., Zimanyi I., Abramson J. J., Pessah I. N. Ryanodine stabilizes multiple conformational states of the skeletal muscle calcium release channel. J Biol Chem. 1992 Nov 25;267(33):23560–23567. [PubMed] [Google Scholar]
  4. Bull R., Marengo J. J., Suárez-Isla B. A., Donoso P., Sutko J. L., Hidalgo C. Activation of calcium channels in sarcoplasmic reticulum from frog muscle by nanomolar concentrations of ryanodine. Biophys J. 1989 Oct;56(4):749–756. doi: 10.1016/S0006-3495(89)82722-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collet C., Allard B., Tourneur Y., Jacquemond V. Intracellular calcium signals measured with indo-1 in isolated skeletal muscle fibres from control and mdx mice. J Physiol. 1999 Oct 15;520(Pt 2):417–429. doi: 10.1111/j.1469-7793.1999.00417.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coronado R., Morrissette J., Sukhareva M., Vaughan D. M. Structure and function of ryanodine receptors. Am J Physiol. 1994 Jun;266(6 Pt 1):C1485–C1504. doi: 10.1152/ajpcell.1994.266.6.C1485. [DOI] [PubMed] [Google Scholar]
  7. Csernoch L., Bernengo J. C., Szentesi P., Jacquemond V. Measurements of intracellular Mg2+ concentration in mouse skeletal muscle fibers with the fluorescent indicator mag-indo-1. Biophys J. 1998 Aug;75(2):957–967. doi: 10.1016/S0006-3495(98)77584-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Franzini-Armstrong C., Protasi F. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev. 1997 Jul;77(3):699–729. doi: 10.1152/physrev.1997.77.3.699. [DOI] [PubMed] [Google Scholar]
  9. Fryer M. W., Lamb G. D., Neering I. R. The action of ryanodine on rat fast and slow intact skeletal muscles. J Physiol. 1989 Jul;414:399–413. doi: 10.1113/jphysiol.1989.sp017695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garcia J., Schneider M. F. Calcium transients and calcium release in rat fast-twitch skeletal muscle fibres. J Physiol. 1993 Apr;463:709–728. doi: 10.1113/jphysiol.1993.sp019618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. García J., Avila-Sakar A. J., Stefani E. Differential effects of ryanodine and tetracaine on charge movement and calcium transients in frog skeletal muscle. J Physiol. 1991;440:403–417. doi: 10.1113/jphysiol.1991.sp018715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gonzalez A., Caputo C. Ryanodine interferes with charge movement repriming in amphibian skeletal muscle fibers. Biophys J. 1996 Jan;70(1):376–382. doi: 10.1016/S0006-3495(96)79581-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. González A., Kirsch W. G., Shirokova N., Pizarro G., Brum G., Pessah I. N., Stern M. D., Cheng H., Ríos E. Involvement of multiple intracellular release channels in calcium sparks of skeletal muscle. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4380–4385. doi: 10.1073/pnas.070056497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Imagawa T., Smith J. S., Coronado R., Campbell K. P. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem. 1987 Dec 5;262(34):16636–16643. [PubMed] [Google Scholar]
  15. Jacquemond V. Indo-1 fluorescence signals elicited by membrane depolarization in enzymatically isolated mouse skeletal muscle fibers. Biophys J. 1997 Aug;73(2):920–928. doi: 10.1016/S0006-3495(97)78124-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Lattanzio F. A., Jr, Schlatterer R. G., Nicar M., Campbell K. P., Sutko J. L. The effects of ryanodine on passive calcium fluxes across sarcoplasmic reticulum membranes. J Biol Chem. 1987 Feb 25;262(6):2711–2718. [PubMed] [Google Scholar]
  18. Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem. 1986 May 15;261(14):6300–6306. [PubMed] [Google Scholar]
  19. 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]
  20. Meissner G., el-Hashem A. Ryanodine as a functional probe of the skeletal muscle sarcoplasmic reticulum Ca2+ release channel. Mol Cell Biochem. 1992 Sep 8;114(1-2):119–123. doi: 10.1007/BF00240306. [DOI] [PubMed] [Google Scholar]
  21. Oyamada H., Iino M., Endo M. Effects of ryanodine on the properties of Ca2+ release from the sarcoplasmic reticulum in skinned skeletal muscle fibres of the frog. J Physiol. 1993 Oct;470:335–348. doi: 10.1113/jphysiol.1993.sp019861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pessah I. N., Stambuk R. A., Casida J. E. Ca2+-activated ryanodine binding: mechanisms of sensitivity and intensity modulation by Mg2+, caffeine, and adenine nucleotides. Mol Pharmacol. 1987 Mar;31(3):232–238. [PubMed] [Google Scholar]
  23. Rousseau E., Smith J. S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol. 1987 Sep;253(3 Pt 1):C364–C368. doi: 10.1152/ajpcell.1987.253.3.C364. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Shirokova N., García J., Pizarro G., Ríos E. Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol. 1996 Jan;107(1):1–18. doi: 10.1085/jgp.107.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Smith J. S., Imagawa T., Ma J., Fill M., Campbell K. P., Coronado R. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J Gen Physiol. 1988 Jul;92(1):1–26. doi: 10.1085/jgp.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Su J. Y. Effects of ryanodine on skinned skeletal muscle fibers of the rabbit. Pflugers Arch. 1987 Nov;410(4-5):510–516. doi: 10.1007/BF00586534. [DOI] [PubMed] [Google Scholar]
  28. Sutko J. L., Airey J. A., Welch W., Ruest L. The pharmacology of ryanodine and related compounds. Pharmacol Rev. 1997 Mar;49(1):53–98. [PubMed] [Google Scholar]
  29. Szentesi P., Jacquemond V., Kovács L., Csernoch L. Intramembrane charge movement and sarcoplasmic calcium release in enzymatically isolated mammalian skeletal muscle fibres. J Physiol. 1997 Dec 1;505(Pt 2):371–384. doi: 10.1111/j.1469-7793.1997.371bb.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Timmer J., Müller T., Melzer W. Numerical methods to determine calcium release flux from calcium transients in muscle cells. Biophys J. 1998 Apr;74(4):1694–1707. doi: 10.1016/S0006-3495(98)77881-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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