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. 1986 Apr;373:481–511. doi: 10.1113/jphysiol.1986.sp016059

Intramembrane charge movement and calcium release in frog skeletal muscle.

W Melzer, M F Schneider, B J Simon, G Szucs
PMCID: PMC1182549  PMID: 3489092

Abstract

Intramembrane charge movement and myoplasmic free calcium transients (delta[Ca2+]) were monitored in voltage-clamped segments of isolated frog muscle fibres cut at both ends and mounted in a double Vaseline-gap chamber. The fibres were stretched to sarcomere lengths of 3.5-4.6 micron to minimize mechanical movement and the related optical artifacts. The over-all calcium removal capability of each fibre was characterized by analysing the decay of delta[Ca2+] following pulses of several different amplitudes and durations. The rate of sarcoplasmic reticulum (s.r.) calcium release was then calculated for each delta[Ca2+] using the calcium removal properties determined for that fibre. The calculated calcium release wave form reached a relatively early peak and then declined appreciably during a 100-150 ms depolarizing pulse. The voltage dependence of the peak rate of calcium release was steeper and was centred at more positive membrane potentials than the steady-state voltage dependence of charge movement in the same fibres. A considerable fraction of the total intramembrane charge was moved at potentials at which delta[Ca2+] and calcium release were only a few per cent of maximum. This 'subthreshold' charge may correspond to charge moved in preliminary transitions that precede a final charge transition that activates release. A 'stepped on' pulse protocol was used to experimentally separate the subthreshold charge movement from the charge movement of the final transitions that may control calcium release. The stepped on pulse consisted of a set 50 ms pre-pulse to a potential just at or below the potential for detectable delta[Ca2+] followed immediately by a test pulse of varying amplitude and duration. For a wide range of test pulse amplitudes and durations in the stepped on protocol the peak rate of calcium release was linearly related to the charge movement during the test pulse. This result points to a tight control of activation of s.r. calcium release by intramembrane charge movement. The voltage dependence of both charge movement and of the rate of calcium release could be fitted simultaneously with a three-state, two-transition sequential model in which charge moves in both transitions but only the final transition activates s.r. calcium release. A model with three identical and independent charged gating particles per channel gave an equally good fit to the data. Both models closely fit the charge movement and release data except within about 10 mV of the voltage at which release became detectable, where release varied more steeply with membrane potential than predicted by either model.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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

  1. Adrian R. H., Chandler W. K., Hodgkin A. L. The kinetics of mechanical activation in frog muscle. J Physiol. 1969 Sep;204(1):207–230. doi: 10.1113/jphysiol.1969.sp008909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Chandler W. K., Rakowski R. F. Charge movement and mechanical repriming in skeletal muscle. J Physiol. 1976 Jan;254(2):361–388. doi: 10.1113/jphysiol.1976.sp011236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Armstrong C. M. Sodium channels and gating currents. Physiol Rev. 1981 Jul;61(3):644–683. doi: 10.1152/physrev.1981.61.3.644. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Caputo C. The effect of low temperature on the excitation-contraction coupling phenomena of frog single muscle fibres. J Physiol. 1972 Jun;223(2):461–482. doi: 10.1113/jphysiol.1972.sp009858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caputo C. The time course of potassium contractures of single muscle fibres. J Physiol. 1972 Jun;223(2):483–505. doi: 10.1113/jphysiol.1972.sp009859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chandler W. K., Rakowski R. F., Schneider M. F. A non-linear voltage dependent charge movement in frog skeletal muscle. J Physiol. 1976 Jan;254(2):245–283. doi: 10.1113/jphysiol.1976.sp011232. [DOI] [PMC free article] [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. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HODGKIN A. L., HOROWICZ P. Potassium contractures in single muscle fibres. J Physiol. 1960 Sep;153:386–403. doi: 10.1113/jphysiol.1960.sp006541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Huang C. L. Pharmacological separation of charge movement components in frog skeletal muscle. J Physiol. 1982 Mar;324:375–387. doi: 10.1113/jphysiol.1982.sp014118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hui C. S. Pharmacological studies of charge movement in frog skeletal muscle. J Physiol. 1983 Apr;337:509–529. doi: 10.1113/jphysiol.1983.sp014639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kovacs L., Rios E., Schneider M. F. Measurement and modification of free calcium transients in frog skeletal muscle fibres by a metallochromic indicator dye. J Physiol. 1983 Oct;343:161–196. doi: 10.1113/jphysiol.1983.sp014887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Lee K. S., Tsien R. W. High selectivity of calcium channels in single dialysed heart cells of the guinea-pig. J Physiol. 1984 Sep;354:253–272. doi: 10.1113/jphysiol.1984.sp015374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Melzer W., Ríos E., Schneider M. F. The removal of myoplasmic free calcium following calcium release in frog skeletal muscle. J Physiol. 1986 Mar;372:261–292. doi: 10.1113/jphysiol.1986.sp016008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miledi R., Parker I., Zhu P. H. Calcium transients studied under voltage-clamp control in frog twitch muscle fibres. J Physiol. 1983 Jul;340:649–680. doi: 10.1113/jphysiol.1983.sp014785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Palade P., Vergara J. Arsenazo III and antipyrylazo III calcium transients in single skeletal muscle fibers. J Gen Physiol. 1982 Apr;79(4):679–707. doi: 10.1085/jgp.79.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Scarpa A., Brinley F. J., Jr, Dubyak G. Antipyrylazo III, a "middle range" Ca2+ metallochromic indicator. Biochemistry. 1978 Apr 18;17(8):1378–1386. doi: 10.1021/bi00601a004. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Schneider M. F., Rios E., Melzer W. Use of a metallochromic indicator to study intracellular calcium movements in skeletal muscle. Cell Calcium. 1985 Apr;6(1-2):109–118. doi: 10.1016/0143-4160(85)90038-7. [DOI] [PubMed] [Google Scholar]
  29. Stimers J. R., Bezanilla F., Taylor R. E. Sodium channel activation in the squid giant axon. Steady state properties. J Gen Physiol. 1985 Jan;85(1):65–82. doi: 10.1085/jgp.85.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]

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