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PMID: 8202554 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Membrane repolarization stops caffeine-induced Ca2+ release in skeletal muscle cells.

Suda N, Penner R

Abstract

We have combined the patch-clamp technique with fura-2 measurements to investigate whether the Ca(2+)-induced Ca(2+)-release channel is under the control of membrane potential in rat skeletal myoballs. We report that Ca2+ release induced by 10 mM caffeine is turned off by membrane repolarization, a phenomenon that we term RISC (repolarization-induced stop of Ca2+ release). The RISC phenomenon is voltage- and time-dependent. It is evident only when the release channels are first transferred into a functionally "voltage-activated" state through membrane depolarization. The results demonstrate that membrane repolarization actively closes the caffeine-activated release channels and suggest that the ryanodine receptor is actually the physiological depolarization-induced Ca(2+)-release channel. Thus, our data provide compelling evidence for a bidirectional voltage control (depolarization and repolarization) of the Ca(2+)-release channel in the sarcoplasmic reticulum by a voltage sensor in the transverse tubule membrane.

MeSH Terms
Animals Animals, Newborn Caffeine/pharmacology Calcium/metabolism Calcium Channels/physiology Cells, Cultured In Vitro Techniques Ion Channel Gating/drug effects Membrane Potentials Muscle Proteins/physiology Muscles/metabolism Rats Ryanodine Receptor Calcium Release Channel Sarcoplasmic Reticulum/physiology Time Factors
Chemicals
Calcium Channels Muscle Proteins Ryanodine Receptor Calcium Release Channel Caffeine Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Suda N
Max-Planck-Institut für biophysikalische Chemie, Göttingen, Germany.
Penner R
References (40)
40 references, click to expand
  1. Elemental distribution in striated muscle and the effects of hypertonicity. Electron probe analysis of cryo sections.
    J Cell Biol. 1977 Sep;74(3):828-57 PMID: 302837
  2. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  3. 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):16636-43 PMID: 2445748
  4. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA.
    Nature. 1988 Nov 10;336(6195):134-9 PMID: 2903448
  5. Regenerative calcium release within muscle cells.
    Science. 1970 Jan 2;167(3914):58-9 PMID: 5409477
  6. Excitation-contraction coupling and the mechanism of muscle contraction.
    Annu Rev Physiol. 1991;53:1-16 PMID: 2042955
  7. 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 PMID: 2848455
  8. STUDIES OF THE TRIAD : I. Structure of the Junction in Frog Twitch Fibers.
    J Cell Biol. 1970 Nov 1;47(2):488-99 PMID: 19866746
  9. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig.
    J Physiol. 1987 Mar;384:199-222 PMID: 2443659
  10. Effect of postnatal development on calcium currents and slow charge movement in mammalian skeletal muscle.
    J Gen Physiol. 1988 Jun;91(6):799-815 PMID: 2458430
  11. Voltage sensor of excitation-contraction coupling in skeletal muscle.
    Physiol Rev. 1991 Jul;71(3):849-908 PMID: 2057528
  12. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle.
    J Biol Chem. 1987 Feb 5;262(4):1740-7 PMID: 3805051
  13. 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):333-70 PMID: 8228914
  14. Voltage-independent calcium release in heart muscle.
    Science. 1990 Oct 26;250(4980):565-8 PMID: 2173135
  15. Effects of glycerol treatment and maintained depolarization on charge movement in skeletal muscle.
    J Physiol. 1976 Jan;254(2):285-316 PMID: 1082507
  16. Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad.
    J Physiol. 1991 Mar;434:507-28 PMID: 1708823
  17. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum.
    J Gen Physiol. 1988 Jul;92(1):1-26 PMID: 2459298
  18. Calcium release and sarcoplasmic reticulum membrane potential in frog skeletal muscle fibres.
    J Physiol. 1984 Mar;348:209-38 PMID: 6716284
  19. Mechanism of calcium release from skeletal sarcoplasmic reticulum.
    J Membr Biol. 1982;66(3):193-201 PMID: 6284941
  20. The effects of calcium deprivation upon mechanical and electrophysiological parameters in skeletal muscle fibres of the frog.
    J Physiol. 1979 Nov;296:411-29 PMID: 316821
  21. Calcium currents in embryonic and neonatal mammalian skeletal muscle.
    J Gen Physiol. 1988 Jun;91(6):781-98 PMID: 2458429
  22. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  23. 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):681-5 PMID: 2440542
  24. Purification and reconstitution of the calcium release channel from skeletal muscle.
    Nature. 1988 Jan 28;331(6154):315-9 PMID: 2448641
  25. Calcium gradients and buffers in bovine chromaffin cells.
    J Physiol. 1992 May;450:273-301 PMID: 1331424
  26. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling.
    Nature. 1973 Mar 23;242(5395):244-6 PMID: 4540479
  27. Ca2+ transients in cardiac myocytes measured with high and low affinity Ca2+ indicators.
    Biophys J. 1993 Oct;65(4):1632-47 PMID: 8274651
  28. Effect of caffeine on intramembrane charge movement and calcium transients in cut skeletal muscle fibres of the frog.
    J Physiol. 1983 Aug;341:559-78 PMID: 6604806
  29. Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides.
    Biochemistry. 1986 Jan 14;25(1):236-44 PMID: 3754147
  30. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle.
    Nature. 1987 Feb 19-25;325(6106):717-20 PMID: 2434854
  31. Progressive predominance of 'skeletal' versus 'cardiac' types of excitation-contraction coupling during in vitro skeletal myogenesis.
    Pflugers Arch. 1992 Nov;422(2):207-9 PMID: 1488277
  32. Calcium dependence of inactivation of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers.
    J Gen Physiol. 1991 Mar;97(3):437-71 PMID: 2037837
  33. Slow inward calcium currents have no obvious role in muscle excitation-contraction coupling.
    Nature. 1982 Jul 15;298(5871):292-4 PMID: 6806669
  34. Twitches in the presence of ethylene glycol bis( -aminoethyl ether)-N,N'-tetracetic acid.
    Biochim Biophys Acta. 1972 Jun 23;267(3):605-8 PMID: 4537984
  35. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate.
    Nature. 1987 May 21-27;327(6119):249-52 PMID: 3494954
  36. Fura-2 calcium transients in frog skeletal muscle fibres.
    J Physiol. 1988 Sep;403:151-92 PMID: 3267019
  37. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs.
    Nature. 1990 Aug 9;346(6284):569-72 PMID: 2165571
  38. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres.
    Nature. 1970 Oct 3;228(5266):34-6 PMID: 5456208
  39. Potassium contractures in single muscle fibres.
    J Physiol. 1960 Sep;153:386-403 PMID: 13714849
  40. A general procedure for determining the rate of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers.
    Biophys J. 1987 Jun;51(6):849-63 PMID: 3496921
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1994-06-07
Pages
5725-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC44069
Subset
IM
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