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. 1991 Dec;444:65–84. doi: 10.1113/jphysiol.1991.sp018866

Excitation-contraction coupling in skeletal muscle fibres of rat and toad in the presence of GTP gamma S.

G D Lamb 1, D G Stephenson 1
PMCID: PMC1179921  PMID: 1726598

Abstract

1. Rapid force responses were elicited in single mechanically skinned fibres from extensor digitorum longus (EDL) muscle of the rat when the fibres were depolarized by substituting K+ in the bathing solution with Na+. The properties of these depolarization-induced responses, the responses to lowered [Mg2+], and the characteristics of the slow prolonged response ('second component') produced in 'loaded' fibres by choline chloride (ChCl) substitution, were virtually identical to those observed previously in skinned fibres from toad muscle. 2. At physiological levels of [Mg2+] (1 mM) and Ca2+ loading, application of 50 microM- to 1 mM-GTP gamma S (guanosine-5'-O-(3-thiotriphosphate), a non-hydrolysable analogue of GTP) did not produce a response in any mammalian or amphibian fibre, even though the depolarization-induced coupling was totally functional. Furthermore, the presence of GTP gamma S had no apparent effect on the size, the threshold or the maximum number of responses which could be elicited by depolarization. 3. GTP gamma S did not elicit any response when excitation-contraction coupling was abolished by prolonged depolarization or by chemically skinning the fibre with saponin or by 24 h exposure to low [Ca2+] (5 mM-EGTA). 4. GDP beta S (guanosine-5'-O-(2-thiodiphosphate), 250 microM or 1 mM) neither evoked a response nor affected the responses to depolarization or caffeine. 5. When the [Mg2+] was lowered to 0.2 mM and the fibres were heavily loaded with Ca2+, addition of GTP gamma S (250 microM or 1 mM) induced a small response in about 50% of fibres, but depolarization-induced responses were not affected in any fibres. 6. Asymmetric charge movement recorded in EDL fibres with the vaseline-gap voltage clamp was not affected by the application of 1 mM-GTP gamma S to the cut ends of the fibres for up to 1 h. 7. These data imply that GTP-binding proteins (G-proteins) are not involved in coupling the voltage sensors to Ca2+ release in skeletal muscle. Furthermore, there was no evidence that G-proteins play any role in modulating the voltage sensors, though this possibility could not be totally excluded.

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Selected References

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  1. Armstrong C. M., Bezanilla F. M., Horowicz P. Twitches in the presence of ethylene glycol bis( -aminoethyl ether)-N,N'-tetracetic acid. Biochim Biophys Acta. 1972 Jun 23;267(3):605–608. doi: 10.1016/0005-2728(72)90194-6. [DOI] [PubMed] [Google Scholar]
  2. Arreola J., Calvo J., García M. C., Sánchez J. A. Modulation of calcium channels of twitch skeletal muscle fibres of the frog by adrenaline and cyclic adenosine monophosphate. J Physiol. 1987 Dec;393:307–330. doi: 10.1113/jphysiol.1987.sp016825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Di Virgilio F., Salviati G., Pozzan T., Volpe P. Is a guanine nucleotide-binding protein involved in excitation-contraction coupling in skeletal muscle? EMBO J. 1986 Feb;5(2):259–262. doi: 10.1002/j.1460-2075.1986.tb04207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Donaldson S. K. Peeled mammalian skeletal muscle fibers. Possible stimulation of Ca2+ release via a transverse tubule-sarcoplasmic reticulum mechanism. J Gen Physiol. 1985 Oct;86(4):501–525. doi: 10.1085/jgp.86.4.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dulhunty A. F., Gage P. W. Asymmetrical charge movement in slow- and fast-twitch mammalian muscle fibres in normal and paraplegic rats. J Physiol. 1983 Aug;341:213–231. doi: 10.1113/jphysiol.1983.sp014802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. García J., Gamboa-Aldeco R., Stefani E. Charge movement and calcium currents in skeletal muscle fibers are enhanced by GTP gamma S. Pflugers Arch. 1990 Sep;417(1):114–116. doi: 10.1007/BF00370779. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Huang C. L. Voltage-dependent block of charge movement components by nifedipine in frog skeletal muscle. J Gen Physiol. 1990 Sep;96(3):535–557. doi: 10.1085/jgp.96.3.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hui C. S. D600 binding sites on voltage-sensors for excitation-contraction coupling in frog skeletal muscle are intracellular. J Muscle Res Cell Motil. 1990 Dec;11(6):471–488. doi: 10.1007/BF01745215. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Lamb G. D. Ca2+ channels or voltage sensors? Nature. 1991 Jul 11;352(6331):113–113. doi: 10.1038/352113b0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Lamb G. D., Stephenson D. G. Calcium release in skinned muscle fibres of the toad by transverse tubule depolarization or by direct stimulation. J Physiol. 1990 Apr;423:495–517. doi: 10.1113/jphysiol.1990.sp018036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lamb G. D., Stephenson D. G. Control of calcium release and the effect of ryanodine in skinned muscle fibres of the toad. J Physiol. 1990 Apr;423:519–542. doi: 10.1113/jphysiol.1990.sp018037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lamb G. D., Stephenson D. G. Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. J Physiol. 1991 Mar;434:507–528. doi: 10.1113/jphysiol.1991.sp018483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lamb G. D., Walsh T. Calcium currents, charge movement and dihydropyridine binding in fast- and slow-twitch muscles of rat and rabbit. J Physiol. 1987 Dec;393:595–617. doi: 10.1113/jphysiol.1987.sp016843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Shuba Y. M., Hesslinger B., Trautwein W., McDonald T. F., Pelzer D. Whole-cell calcium current in guinea-pig ventricular myocytes dialysed with guanine nucleotides. J Physiol. 1990 May;424:205–228. doi: 10.1113/jphysiol.1990.sp018063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Somasundaram B., Tregear R. T., Trentham D. R. GTP gamma S causes contraction of skinned frog skeletal muscle via the DHP-sensitive Ca2+ channels of sealed T-tubules. Pflugers Arch. 1991 Mar;418(1-2):137–143. doi: 10.1007/BF00370462. [DOI] [PubMed] [Google Scholar]
  23. Stephenson D. G., Wendt I. R., Forrest Q. G. Non-uniform ion distributions and electrical potentials in sarcoplasmic regions of skeletal muscle fibres. Nature. 1981 Feb 19;289(5799):690–692. doi: 10.1038/289690a0. [DOI] [PubMed] [Google Scholar]
  24. Stephenson D. G., Williams D. A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J Physiol. 1981 Aug;317:281–302. doi: 10.1113/jphysiol.1981.sp013825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tanabe T., Beam K. G., Powell J. A., Numa S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature. 1988 Nov 10;336(6195):134–139. doi: 10.1038/336134a0. [DOI] [PubMed] [Google Scholar]
  26. Taylor C. W. The role of G proteins in transmembrane signalling. Biochem J. 1990 Nov 15;272(1):1–13. doi: 10.1042/bj2720001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Toutant M., Gabrion J., Vandaele S., Peraldi-Roux S., Barhanin J., Bockaert J., Rouot B. Cellular distribution and biochemical characterization of G proteins in skeletal muscle: comparative location with voltage-dependent calcium channels. EMBO J. 1990 Feb;9(2):363–369. doi: 10.1002/j.1460-2075.1990.tb08119.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Villaz M., Robert M., Carrier L., Beeler T., Rouot B., Toutant M., Dupont Y. G-protein dependent potentiation of calcium release from sarcoplasmic reticulum of skeletal muscle. Cell Signal. 1989;1(5):493–506. doi: 10.1016/0898-6568(89)90034-x. [DOI] [PubMed] [Google Scholar]
  29. Yatani A., Imoto Y., Codina J., Hamilton S. L., Brown A. M., Birnbaumer L. The stimulatory G protein of adenylyl cyclase, Gs, also stimulates dihydropyridine-sensitive Ca2+ channels. Evidence for direct regulation independent of phosphorylation by cAMP-dependent protein kinase or stimulation by a dihydropyridine agonist. J Biol Chem. 1988 Jul 15;263(20):9887–9895. [PubMed] [Google Scholar]

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