Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Apr;398:475–505. doi: 10.1113/jphysiol.1988.sp017053

Voltage sensors of the frog skeletal muscle membrane require calcium to function in excitation-contraction coupling.

G Brum 1, R Fitts 1, G Pizarro 1, E Ríos 1
PMCID: PMC1191783  PMID: 3260626

Abstract

1. Intramembrane charge movements and changes in intracellular Ca2+ concentration (Ca2+ transients) elicited by pulse depolarization were measured in frog fast twitch cut muscle fibres under voltage clamp. 2. Extracellular solutions with very low [Ca2+] and 2 mM-Mg2+ , shown in the previous paper to reduce Ca2+ release from the sarcoplasmic reticulum (SR), were found to cause two changes in charge movement: (a) a decrease (-12 nC/microF) in the charge that moves during depolarizing pulses from -90 to 0 mV, termed here 'charge 1'; (b) an increase (+7 nC/microF) in the charge moved by hyperpolarizing pulses from -90 to -180 mV, termed 'charge 2'. 3. The increase in charge moved by hyperpolarizing pulses was correlated (r = 0.64) with the decrease in charge moved by depolarizing pulses and both were correlated with the inhibition of Ca2+ release recorded in the same fibres. 4. The low Ca2+ solutions caused a shift to more negative voltages of the dependence relating charge movement and holding potential (VH). This shift is of similar magnitude (about 22 mV) and direction as the shift in the curve relating Ca2+ release flux to VH (previous paper). 5. In solutions with normal [Ca2+] a conditioning depolarization to 0 mV, of 2 s duration, placed 100 ms before a test pulse from -70 to 0 mV, reduced by 30% the amount of charge displaced by the test pulse. Conditioning pulses of 1 s or less caused potentiation of charge movement by up to 30%. 6. In low Ca2+ solutions, reduction of charge was observed at all durations of the conditioning pulse. The duration for half-inhibition was near 200 ms. 7. An extracellular solution with no metal cations caused a more radical inhibition than the low Ca2+ solutions that contained Mg2+. The inhibition of Ca2+ release was essentially complete (90-100%). The charge moved by a pulse to 0 mV was reduced by 20 nC/microF and the charge moved by a pulse to -170 mV increased 8 nC/microF. This shows that Mg2+ supports excitation-contraction (E-C) coupling to some extent. 8. A state model of the voltage sensor of E-C coupling explains qualitatively the observations in both papers.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
475

Selected References

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

  1. Adrian R. H., Peres A. Charge movement and membrane capacity in frog muscle. J Physiol. 1979 Apr;289:83–97. doi: 10.1113/jphysiol.1979.sp012726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong C. M., Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol. 1977 Nov;70(5):567–590. doi: 10.1085/jgp.70.5.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrett N., Barrett E. F. Excitation-contraction coupling in skeletal muscle: blockade by high extracellular concentrations of calcium buffers. Science. 1978 Jun 16;200(4347):1270–1272. doi: 10.1126/science.96524. [DOI] [PubMed] [Google Scholar]
  4. Berwe D., Gottschalk G., Lüttgau H. C. Effects of the calcium antagonist gallopamil (D600) upon excitation-contraction coupling in toe muscle fibres of the frog. J Physiol. 1987 Apr;385:693–707. doi: 10.1113/jphysiol.1987.sp016515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bezanilla F., Taylor R. E., Fernández J. M. Distribution and kinetics of membrane dielectric polarization. 1. Long-term inactivation of gating currents. J Gen Physiol. 1982 Jan;79(1):21–40. doi: 10.1085/jgp.79.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brum G., Rios E. Intramembrane charge movement in frog skeletal muscle fibres. Properties of charge 2. J Physiol. 1987 Jun;387:489–517. doi: 10.1113/jphysiol.1987.sp016586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Caillé J., Ildefonse M., Rougier O. Excitation-contraction coupling in skeletal muscle. Prog Biophys Mol Biol. 1985;46(3):185–239. doi: 10.1016/0079-6107(85)90009-4. [DOI] [PubMed] [Google Scholar]
  9. Chandler W. K., Rakowski R. F., Schneider M. F. Effects of glycerol treatment and maintained depolarization on charge movement in skeletal muscle. J Physiol. 1976 Jan;254(2):285–316. doi: 10.1113/jphysiol.1976.sp011233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Csernoch L., Kovács L., Szücs G. Perchlorate and the relationship between charge movement and contractile activation in frog skeletal muscle fibres. J Physiol. 1987 Sep;390:213–227. doi: 10.1113/jphysiol.1987.sp016695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Curtis B. A., Eisenberg R. S. Calcium influx in contracting and paralyzed frog twitch muscle fibers. J Gen Physiol. 1985 Mar;85(3):383–408. doi: 10.1085/jgp.85.3.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eisenberg R. S., McCarthy R. T., Milton R. L. Paralysis of frog skeletal muscle fibres by the calcium antagonist D-600. J Physiol. 1983 Aug;341:495–505. doi: 10.1113/jphysiol.1983.sp014819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Graf F., Schatzmann H. J. Some effects of removal of external calcium on pig striated muscle. J Physiol. 1984 Apr;349:1–13. doi: 10.1113/jphysiol.1984.sp015138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hollingworth S., Marshall M. W. A comparative study of charge movement in rat and frog skeletal muscle fibres. J Physiol. 1981 Dec;321:583–602. doi: 10.1113/jphysiol.1981.sp014004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horowicz P., Schneider M. F. Membrane charge moved at contraction thresholds in skeletal muscle fibres. J Physiol. 1981 May;314:595–633. doi: 10.1113/jphysiol.1981.sp013726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Horowicz P., Schneider M. F. Membrane charge movement in contracting and non-contracting skeletal muscle fibres. J Physiol. 1981 May;314:565–593. doi: 10.1113/jphysiol.1981.sp013725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hui C. S. Differential properties of two charge components in frog skeletal muscle. J Physiol. 1983 Apr;337:531–552. doi: 10.1113/jphysiol.1983.sp014640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hui C. S., Milton R. L., Eisenberg R. S. Charge movement in skeletal muscle fibers paralyzed by the calcium-entry blocker D600. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2582–2585. doi: 10.1073/pnas.81.8.2582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kovács L., Ríos E., Schneider M. F. Calcium transients and intramembrane charge movement in skeletal muscle fibres. Nature. 1979 May 31;279(5712):391–396. doi: 10.1038/279391a0. [DOI] [PubMed] [Google Scholar]
  20. Lamb G. D. Asymmetric charge movement in polarized and depolarized muscle fibres of the rabbit. J Physiol. 1987 Feb;383:349–367. doi: 10.1113/jphysiol.1987.sp016413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lamb G. D. Components of charge movement in rabbit skeletal muscle: the effect of tetracaine and nifedipine. J Physiol. 1986 Jul;376:85–100. doi: 10.1113/jphysiol.1986.sp016143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lüttgau H. C., Gottschalk G., Berwe D. The effect of calcium and Ca antagonists upon excitation-contraction coupling. Can J Physiol Pharmacol. 1987 Apr;65(4):717–723. doi: 10.1139/y87-118. [DOI] [PubMed] [Google Scholar]
  23. Lüttgau H. C., Spiecker W. The effects of calcium deprivation upon mechanical and electrophysiological parameters in skeletal muscle fibres of the frog. J Physiol. 1979 Nov;296:411–429. doi: 10.1113/jphysiol.1979.sp013013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLaughlin S. G., Szabo G., Eisenman G. Divalent ions and the surface potential of charged phospholipid membranes. J Gen Physiol. 1971 Dec;58(6):667–687. doi: 10.1085/jgp.58.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Melzer W., Rios E., Schneider M. F. A general procedure for determining the rate of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. Biophys J. 1987 Jun;51(6):849–863. doi: 10.1016/S0006-3495(87)83413-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Melzer W., Schneider M. F., Simon B. J., Szucs G. Intramembrane charge movement and calcium release in frog skeletal muscle. J Physiol. 1986 Apr;373:481–511. doi: 10.1113/jphysiol.1986.sp016059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rakowski R. F., Best P. M., James-Kracke M. R. Voltage dependence of membrane charge movement and calcium release in frog skeletal muscle fibres. J Muscle Res Cell Motil. 1985 Aug;6(4):403–433. doi: 10.1007/BF00712580. [DOI] [PubMed] [Google Scholar]
  29. Rios E., Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 1987 Feb 19;325(6106):717–720. doi: 10.1038/325717a0. [DOI] [PubMed] [Google Scholar]
  30. Schneider M. F., Chandler W. K. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature. 1973 Mar 23;242(5395):244–246. doi: 10.1038/242244a0. [DOI] [PubMed] [Google Scholar]
  31. Simon B. J., Beam K. G. Slow charge movement in mammalian skeletal muscle. J Gen Physiol. 1985 Jan;85(1):1–19. doi: 10.1085/jgp.85.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES