Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1989 Mar 1;93(3):565–584. doi: 10.1085/jgp.93.3.565

Anatomical distribution of voltage-dependent membrane capacitance in frog skeletal muscle fibers

PMCID: PMC2216213  PMID: 2784827

Abstract

Components of nonlinear capacitance, or charge movement, were localized in the membranes of frog skeletal muscle fibers by studying the effect of 'detubulation' resulting from sudden withdrawal of glycerol from a glycerol-hypertonic solution in which the muscles had been immersed. Linear capacitance was evaluated from the integral of the transient current elicited by imposed voltage clamp steps near the holding potential using bathing solutions that minimized tubular voltage attenuation. The dependence of linear membrane capacitance on fiber diameter in intact fibers was consistent with surface and tubular capacitances and a term attributable to the capacitance of the fiber end. A reduction in this dependence in detubulated fibers suggested that sudden glycerol withdrawal isolated between 75 and 100% of the transverse tubules from the fiber surface. Glycerol withdrawal in two stages did not cause appreciable detubulation. Such glycerol-treated but not detubulated fibers were used as controls. Detubulation reduced delayed (q gamma) charging currents to an extent not explicable simply in terms of tubular conduction delays. Nonlinear membrane capacitance measured at different voltages was expressed normalized to accessible linear fiber membrane capacitance. In control fibers it was strongly voltage dependent. Both the magnitude and steepness of the function were markedly reduced by adding tetracaine, which removed a component in agreement with earlier reports for q gamma charge. In contrast, detubulated fibers had nonlinear capacitances resembling those of q beta charge, and were not affected by adding tetracaine. These findings are discussed in terms of a preferential localization of tetracaine- sensitive (q gamma) charge in transverse tubule membrane, in contrast to a more even distribution of the tetracaine-resistant (q beta) charge in both transverse tubule and surface membranes. These results suggest that q beta and q gamma are due to different molecules and that the movement of q gamma in the transverse tubule membrane is the voltage- sensing step in excitation-contraction coupling.

Full Text

The Full Text of this article is available as a PDF (1.3 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. Charge movement in the membrane of striated muscle. J Physiol. 1976 Jan;254(2):339–360. doi: 10.1113/jphysiol.1976.sp011235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Almers W. Membrane capacity measurements on frog skeletal muscle in media of low ion content. J Physiol. 1974 Mar;237(3):573–605. doi: 10.1113/jphysiol.1974.sp010499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Adrian R. H., Chandler W. K., Hodgkin A. L. Voltage clamp experiments in striated muscle fibres. J Physiol. 1970 Jul;208(3):607–644. doi: 10.1113/jphysiol.1970.sp009139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Adrian R. H. Charge movement in the membrane of striated muscle. Annu Rev Biophys Bioeng. 1978;7:85–112. doi: 10.1146/annurev.bb.07.060178.000505. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Adrian R. H., Rakowski R. F. Reactivation of membrane charge movement and delayed potassium conductance in skeletal muscle fibres. J Physiol. 1978 May;278:533–557. doi: 10.1113/jphysiol.1978.sp012323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Argiro V. Excitation-contraction uncoupling of striated muscle fibres by formamide treatment: evidence of detubulation. J Muscle Res Cell Motil. 1981 Sep;2(3):283–294. doi: 10.1007/BF00713267. [DOI] [PubMed] [Google Scholar]
  11. Buckingham J. H., Staehelin L. A. The effect of glycerol on the structure of lecithin membranes; a study by freeze-etching and X-ray diffraction. J Microsc. 1969;90(2):83–106. doi: 10.1111/j.1365-2818.1969.tb00698.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Curtis B. M., Catterall W. A. Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry. 1984 May 8;23(10):2113–2118. doi: 10.1021/bi00305a001. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Dulhunty A. F., Franzini-Armstrong C. The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J Physiol. 1975 Sep;250(3):513–539. doi: 10.1113/jphysiol.1975.sp011068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dulhunty A. F., Gage P. W. Differential effects of glycerol treatment on membrane capacity and excitation-contraction coupling in toad sartorius fibres. J Physiol. 1973 Oct;234(2):373–408. doi: 10.1113/jphysiol.1973.sp010350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Eisenberg B. R., Milton R. L. Muscle fiber termination at the tendon in the frog's sartorius: a stereological study. Am J Anat. 1984 Nov;171(3):273–284. doi: 10.1002/aja.1001710304. [DOI] [PubMed] [Google Scholar]
  19. Eisenberg R. S., Howell J. N., Vaughan P. C. The maintenance of resting potentials in glycerol-treated muscle fibres. J Physiol. 1971 May;215(1):95–102. doi: 10.1113/jphysiol.1971.sp009459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. FUJINO M., YAMAGUCHI T., SUZUKI K. 'Glycerol effect' and the mechanism linking excitation of the plasma membrane with contraction. Nature. 1961 Dec 23;192:1159–1161. doi: 10.1038/1921159a0. [DOI] [PubMed] [Google Scholar]
  21. Franzini-Armstrong C. Membrane particles and transmission at the triad. Fed Proc. 1975 Apr;34(5):1382–1389. [PubMed] [Google Scholar]
  22. Gage P. W., Eisenberg R. S. Action potentials, afterpotentials, and excitation-contraction coupling in frog sartorius fibers without transverse tubules. J Gen Physiol. 1969 Mar;53(3):298–310. doi: 10.1085/jgp.53.3.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gage P. W., Eisenberg R. S. Capacitance of the surface and transverse tubular membrane of frog sartorius muscle fibers. J Gen Physiol. 1969 Mar;53(3):265–278. doi: 10.1085/jgp.53.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hidalgo C., Carrasco M. A., Magendzo K., Jaimovich E. Phosphorylation of phosphatidylinositol by transverse tubule vesicles and its possible role in excitation-contraction coupling. FEBS Lett. 1986 Jun 23;202(1):69–73. doi: 10.1016/0014-5793(86)80651-2. [DOI] [PubMed] [Google Scholar]
  25. Hodgkin A. L., Nakajima S. Analysis of the membrane capacity in frog muscle. J Physiol. 1972 Feb;221(1):121–136. doi: 10.1113/jphysiol.1972.sp009743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hodgkin A. L., Nakajima S. The effect of diameter on the electrical constants of frog skeletal muscle fibres. J Physiol. 1972 Feb;221(1):105–120. doi: 10.1113/jphysiol.1972.sp009742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. 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]
  30. Huang C. L. Dielectric components of charge movements in skeletal muscle. J Physiol. 1981;313:187–205. doi: 10.1113/jphysiol.1981.sp013658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Huang C. L. Effects of local anaesthetics on the relationship between charge movements and contractile thresholds in frog skeletal muscle. J Physiol. 1981 Nov;320:381–391. doi: 10.1113/jphysiol.1981.sp013956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Jaimovich E., Venosa R. A., Shrager P., Horowicz P. Density and distribution of tetrodotoxin receptors in normal and detubulated frog sartorius muscle. J Gen Physiol. 1976 Apr;67(4):399–416. doi: 10.1085/jgp.67.4.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Krolenko S. A. Changes in the T-system of muscle fibres under the influence of influx and efflux of glycerol. Nature. 1969 Mar 8;221(5184):966–968. doi: 10.1038/221966a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Milton R. L., Mathias R. T., Eisenberg R. S. Electrical properties of the myotendon region of frog twitch muscle fibers measured in the frequency domain. Biophys J. 1985 Aug;48(2):253–267. doi: 10.1016/S0006-3495(85)83779-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nakajima S., Nakajima Y., Peachey L. D. Speed of repolarization and morphology of glygerol-treated frog muscle fibres. J Physiol. 1973 Oct;234(2):465–480. doi: 10.1113/jphysiol.1973.sp010355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. 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]
  45. Schwartz L. M., McCleskey E. W., Almers W. Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. 1985 Apr 25-May 1Nature. 314(6013):747–751. doi: 10.1038/314747a0. [DOI] [PubMed] [Google Scholar]
  46. Vergara J., Tsien R. Y., Delay M. Inositol 1,4,5-trisphosphate: a possible chemical link in excitation-contraction coupling in muscle. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6352–6356. doi: 10.1073/pnas.82.18.6352. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES