Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1991 May 1;97(5):913–947. doi: 10.1085/jgp.97.5.913

The relationship between Q gamma and Ca release from the sarcoplasmic reticulum in skeletal muscle

PMCID: PMC2216505  PMID: 1650812

Abstract

Asymmetric membrane currents and fluxes of Ca2+ release were determined in skeletal muscle fibers voltage clamped in a Vaseline-gap chamber. The conditioning pulse protocol 1 for suppressing Ca2+ release and the "hump" component of charge movement current (I gamma), described in the first paper of this series, was applied at different test pulse voltages. The amplitude of the current suppressed during the ON transient reached a maximum at slightly suprathreshold test voltages (- 50 to -40 mV) and decayed at higher voltages. The component of charge movement current suppressed by 20 microM tetracaine also went through a maximum at low pulse voltages. This anomalous voltage dependence is thus a property of I gamma, defined by either the conditioning protocol or the tetracaine effect. A negative (inward-going) phase was often observed in the asymmetric current during the ON of depolarizing pulses. This inward phase was shown to be an intramembranous charge movement based on (a) its presence in the records of total membrane current, (b) its voltage dependence, with a maximum at slightly suprathreshold voltages, (c) its association with a "hump" in the asymmetric current, (d) its inhibition by interventions that reduce the "hump", (e) equality of ON and OFF areas in the records of asymmetric current presenting this inward phase, and (f) its kinetic relationship with the time derivative of Ca release flux. The nonmonotonic voltage dependence of the amplitude of the hump and the possibility of an inward phase of intramembranous charge movement are used as the main criteria in the quantitative testing of a specific model. According to this model, released Ca2+ binds to negatively charged sites on the myoplasmic face of the voltage sensor and increases the local transmembrane potential, thus driving additional charge movement (the hump). This model successfully predicts the anomalous voltage dependence and all the kinetic properties of I gamma described in the previous papers. It also accounts for the inward phase in total asymmetric current and in the current suppressed by protocol 1. According to this model, I gamma accompanies activating transitions at the same set of voltage sensors as I beta. Therefore it should open additional release channels, which in turn should cause more I gamma, providing a positive feedback mechanism in the regulation of calcium release.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. Adrian R. H., Almers W. The voltage dependence of membrane capacity. J Physiol. 1976 Jan;254(2):317–338. doi: 10.1113/jphysiol.1976.sp011234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Huang C. L. Charge movements near the mechanical threshold in skeletal muscle of Rana temporaria. J Physiol. 1984 Apr;349:483–500. doi: 10.1113/jphysiol.1984.sp015169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adrian R. H., Huang C. L. Experimental analysis of the relationship between charge movement components in skeletal muscle of Rana temporaria. J Physiol. 1984 Aug;353:419–434. doi: 10.1113/jphysiol.1984.sp015344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Adrian R. H., Peres A. R. A gating signal for the potassium channel? Nature. 1977 Jun 30;267(5614):800–804. doi: 10.1038/267800a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Almers W. Some dielectric properties of muscle membrane and their possible importance for excitation-contraction coupling. Ann N Y Acad Sci. 1975 Dec 30;264:278–292. doi: 10.1111/j.1749-6632.1975.tb31489.x. [DOI] [PubMed] [Google Scholar]
  7. Brum G., Fitts R., Pizarro G., Ríos E. Voltage sensors of the frog skeletal muscle membrane require calcium to function in excitation-contraction coupling. J Physiol. 1988 Apr;398:475–505. doi: 10.1113/jphysiol.1988.sp017053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Chandler W. K., Hui C. S. Membrane capacitance in frog cut twitch fibers mounted in a double vaseline-gap chamber. J Gen Physiol. 1990 Aug;96(2):225–256. doi: 10.1085/jgp.96.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Csernoch L., Huang C. L., Szucs G., Kovacs L. Differential effects of tetracaine on charge movements and Ca2+ signals in frog skeletal muscle. J Gen Physiol. 1988 Nov;92(5):601–612. doi: 10.1085/jgp.92.5.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Csernoch L., Pizarro G., Uribe I., Rodríguez M., Ríos E. Interfering with calcium release suppresses I gamma, the "hump" component of intramembranous charge movement in skeletal muscle. J Gen Physiol. 1991 May;97(5):845–884. doi: 10.1085/jgp.97.5.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Duane S., Huang C. L. A quantitative description of the voltage-dependent capacitance in frog skeletal muscle in terms of equilibrium statistical mechanics. Proc R Soc Lond B Biol Sci. 1982 Apr 22;215(1198):75–94. doi: 10.1098/rspb.1982.0029. [DOI] [PubMed] [Google Scholar]
  13. García J., Pizarro G., Ríos E., Stefani E. Effect of the calcium buffer EGTA on the "hump" component of charge movement in skeletal muscle. J Gen Physiol. 1991 May;97(5):885–896. doi: 10.1085/jgp.97.5.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heiny J. A., Jong D., Bryant S. H., Conte-Camerino D., Tortorella V. Enantiomeric effects on excitation-contraction coupling in frog skeletal muscle by a chiral phenoxy carboxylic acid. Biophys J. 1990 Jan;57(1):147–152. doi: 10.1016/S0006-3495(90)82515-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Hollingworth S., Marshall M. W., Robson E. The effects of tetracaine on charge movement in fast twitch rat skeletal muscle fibres. J Physiol. 1990 Feb;421:633–644. doi: 10.1113/jphysiol.1990.sp017966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huang C. L. 'Off' tails of intramembrane charge movements in frog skeletal muscle in perchlorate-containing solutions. J Physiol. 1987 Mar;384:491–509. doi: 10.1113/jphysiol.1987.sp016466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Huang C. L. Analysis of 'off' tails of intramembrane charge movements in skeletal muscle of Rana temporaria. J Physiol. 1984 Nov;356:375–390. doi: 10.1113/jphysiol.1984.sp015471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huang C. L. Intramembrane charge movements in skeletal muscle. Physiol Rev. 1988 Oct;68(4):1197–1147. doi: 10.1152/physrev.1988.68.4.1197. [DOI] [PubMed] [Google Scholar]
  20. Huang C. L., Peachey L. D. Anatomical distribution of voltage-dependent membrane capacitance in frog skeletal muscle fibers. J Gen Physiol. 1989 Mar;93(3):565–584. doi: 10.1085/jgp.93.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Huang C. L. The differential effects of twitch potentiators on charge movements in frog skeletal muscle. J Physiol. 1986 Nov;380:17–33. doi: 10.1113/jphysiol.1986.sp016269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hui C. S., Chandler W. K. Intramembranous charge movement in frog cut twitch fibers mounted in a double vaseline-gap chamber. J Gen Physiol. 1990 Aug;96(2):257–297. doi: 10.1085/jgp.96.2.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. Kushmerick M. J., Podolsky R. J. Ionic mobility in muscle cells. Science. 1969 Dec 5;166(3910):1297–1298. doi: 10.1126/science.166.3910.1297. [DOI] [PubMed] [Google Scholar]
  29. Lamb G. D. Asymmetric charge movement in contracting muscle fibres in the rabbit. J Physiol. 1986 Jul;376:63–83. doi: 10.1113/jphysiol.1986.sp016142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. Simon B. J., Beam K. G. The influence of transverse tubular delays on the kinetics of charge movement in mammalian skeletal muscle. J Gen Physiol. 1985 Jan;85(1):21–42. doi: 10.1085/jgp.85.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith P. D., Liesegang G. W., Berger R. L., Czerlinski G., Podolsky R. J. A stopped-flow investigation of calcium ion binding by ethylene glycol bis(beta-aminoethyl ether)-N,N'-tetraacetic acid. Anal Biochem. 1984 Nov 15;143(1):188–195. doi: 10.1016/0003-2697(84)90575-x. [DOI] [PubMed] [Google Scholar]
  36. Szücs G., Csernoch L., Magyar J., Kovács L. Contraction threshold and the "hump" component of charge movement in frog skeletal muscle. J Gen Physiol. 1991 May;97(5):897–911. doi: 10.1085/jgp.97.5.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vergara J., Caputo C. Effects of tetracaine on charge movements and calcium signals in frog skeletal muscle fibers. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1477–1481. doi: 10.1073/pnas.80.5.1477. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES