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. 1987 Dec;393:307–330. doi: 10.1113/jphysiol.1987.sp016825

Modulation of calcium channels of twitch skeletal muscle fibres of the frog by adrenaline and cyclic adenosine monophosphate.

J Arreola 1, J Calvo 1, M C García 1, J A Sánchez 1
PMCID: PMC1192395  PMID: 2451739

Abstract

1. Modulation of fast and slow Ca2+ channels of frog skeletal muscle by adrenaline (10(-6) to 10(-5) M) and cyclic AMP was investigated using intracellular voltage recordings in intact fibres and a voltage-clamp technique in cut fibres. 2. In tetraethylammonium (TEA), Cl(-)-free Ringer solution, adrenaline increased the maximum rate of rise of Ca2+ spikes by 85% and in a similar solution, peak slow Ca2+ current (ICa,s) by 51%. 3. Application of cyclic AMP to the cut ends of fibres, produced a relative increase of ICa,s of ca. 24%. The effect was maintained for ca. 2 h. 4. Changes in the time course of ICa,s were produced by adrenaline and cyclic AMP: the limiting values of time-to-peak current measured as a function of membrane potential were lower (ca. 41% in adrenaline and ca. 34% in cyclic AMP) than those found in control experiments. Also, ICa,s decayed faster in the presence of adrenaline or cyclic AMP. These changes can be explained by exhaustion of Ca2+ in the lumen of transverse tubular system and do not require the assumption of kinetic variations. 5. Fast Ca2+ currents (ICa,f) which could not be blocked by nifedipine were also recorded. Cyclic AMP greatly increased the amplitude of ICa,f but had no obvious effects on ICa,f kinetics. 6. Application of catalytic subunit of cyclic AMP-dependent protein kinase by diffusion or by pressure injection also increased the amplitude of ICa,s and ICa,f. Pressure injection brought about modifications in the time course of ICa,s that cannot be explained by depletion of Ca2+. 7. Mechanical experiments were performed on single fibres. Nominally Ca2+-free solutions prevented the development and the maintenance of positive inotropic effect of adrenaline on twitch tension. Development of twitch potentiation was dependent upon the frequency of stimulation. Adrenaline was practically ineffective if no stimulation was applied. 8. It is concluded that both populations of Ca2+ channels are modulated by adrenergic stimulation probably via cyclic AMP, and that twitch potentiation may be mediated by a Ca2+ entry through Ca2+ channels.

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Selected References

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  1. Almers W., Fink R., Palade P. T. Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. J Physiol. 1981 Mar;312:177–207. doi: 10.1113/jphysiol.1981.sp013623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Almers W., Palade P. T. Slow calcium and potassium currents across frog muscle membrane: measurements with a vaseline-gap technique. J Physiol. 1981 Mar;312:159–176. doi: 10.1113/jphysiol.1981.sp013622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BIANCHI C. P., SHANES A. M. Calcium influx in skeletal muscle at rest, during activity, and during potassium contracture. J Gen Physiol. 1959 Mar 20;42(4):803–815. doi: 10.1085/jgp.42.4.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BOWMAN W. C., GOLDBERG A. A., RAPER C. A comparison between the effects of a tetanus and the effects of sympathomimetic amines on fast- and slow-contracting mammalian muscles. Br J Pharmacol Chemother. 1962 Dec;19:464–484. doi: 10.1111/j.1476-5381.1962.tb01451.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beam K. G., Knudson C. M., Powell J. A. A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells. Nature. 1986 Mar 13;320(6058):168–170. doi: 10.1038/320168a0. [DOI] [PubMed] [Google Scholar]
  6. Bean B. P., Nowycky M. C., Tsien R. W. Beta-adrenergic modulation of calcium channels in frog ventricular heart cells. 1984 Jan 26-Feb 1Nature. 307(5949):371–375. doi: 10.1038/307371a0. [DOI] [PubMed] [Google Scholar]
  7. Bean B. P. Two kinds of calcium channels in canine atrial cells. Differences in kinetics, selectivity, and pharmacology. J Gen Physiol. 1985 Jul;86(1):1–30. doi: 10.1085/jgp.86.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Beaty G. N., Stefani E. Calcium dependent electrical activity in twitch muscle fibres of the frog. Proc R Soc Lond B Biol Sci. 1976 Aug 27;194(1114):141–150. doi: 10.1098/rspb.1976.0070. [DOI] [PubMed] [Google Scholar]
  9. Bezanilla F., Caputo C., DiPolo R., Rojas H. Potassium conductance of the squid giant axon is modulated by ATP. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2743–2745. doi: 10.1073/pnas.83.8.2743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Caswell A. H., Baker S. P., Boyd H., Potter L. T., Garcia M. beta-adrenergic receptor and adenylate cyclase in transverse tubules of skeletal muscle. J Biol Chem. 1978 May 10;253(9):3049–3054. [PubMed] [Google Scholar]
  11. Chiarandini D. J., Sanchez J. A., Stefani E. Effect of calcium withdrawal on mechanical threshold in skeletal muscle fibres of the frog. J Physiol. 1980 Jun;303:153–163. doi: 10.1113/jphysiol.1980.sp013277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cota G., Stefani E. A fast-activated inward calcium current in twitch muscle fibres of the frog (Rana montezume). J Physiol. 1986 Jan;370:151–163. doi: 10.1113/jphysiol.1986.sp015927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Curtis B. M., Catterall W. A. Phosphorylation of the calcium antagonist receptor of the voltage-sensitive calcium channel by cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2528–2532. doi: 10.1073/pnas.82.8.2528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dani J. A., Sanchez J. A., Hille B. Lyotropic anions. Na channel gating and Ca electrode response. J Gen Physiol. 1983 Feb;81(2):255–281. doi: 10.1085/jgp.81.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Flockerzi V., Oeken H. J., Hofmann F., Pelzer D., Cavalié A., Trautwein W. Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel. Nature. 1986 Sep 4;323(6083):66–68. doi: 10.1038/323066a0. [DOI] [PubMed] [Google Scholar]
  16. Gonzalez-Serratos H., Hill L., Valle-Aguilera R. Effects of catecholamines and cyclic amp on excitation--contraction coupling in isolated skeletal muscle fibres of the frog. J Physiol. 1981 Jun;315:267–282. doi: 10.1113/jphysiol.1981.sp013747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hagiwara S., Ozawa S., Sand O. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol. 1975 May;65(5):617–644. doi: 10.1085/jgp.65.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hidalgo C., González M. E., García A. M. Calcium transport in transverse tubules isolated from rabbit skeletal muscle. Biochim Biophys Acta. 1986 Jan 29;854(2):279–286. doi: 10.1016/0005-2736(86)90121-5. [DOI] [PubMed] [Google Scholar]
  20. Hille B., Campbell D. T. An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol. 1976 Mar;67(3):265–293. doi: 10.1085/jgp.67.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. JENDEN D. J., REGER J. F. THE ROLE OF RESTING POTENTIAL CHANGES IN THE CONTRACTILE FAILURE OF FROG SARTORIUS MUSCLES DURING CALCIUM DEPRIVATION. J Physiol. 1963 Dec;169:889–901. doi: 10.1113/jphysiol.1963.sp007302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. KRNJEVIC K., MILEDI R. Some effects produced by adrenaline upon neuromuscular propagation in rats. J Physiol. 1958 Apr 30;141(2):291–304. doi: 10.1113/jphysiol.1958.sp005974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kameyama M., Hofmann F., Trautwein W. On the mechanism of beta-adrenergic regulation of the Ca channel in the guinea-pig heart. Pflugers Arch. 1985 Oct;405(3):285–293. doi: 10.1007/BF00582573. [DOI] [PubMed] [Google Scholar]
  24. Levitan I. B. Phosphorylation of ion channels. J Membr Biol. 1985;87(3):177–190. doi: 10.1007/BF01871217. [DOI] [PubMed] [Google Scholar]
  25. Matteson D. R., Armstrong C. M. Properties of two types of calcium channels in clonal pituitary cells. J Gen Physiol. 1986 Jan;87(1):161–182. doi: 10.1085/jgp.87.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miledi R., Parker I., Zhu P. H. Extracellular ions and excitation-contraction coupling in frog twitch muscle fibres. J Physiol. 1984 Jun;351:687–710. doi: 10.1113/jphysiol.1984.sp015271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moolenaar W. H., Spector I. The calcium action potential and a prolonged calcium dependent after-hyperpolarization in mouse neuroblastoma cells. J Physiol. 1979 Jul;292:297–306. doi: 10.1113/jphysiol.1979.sp012851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Oota I., Nagai T. Effects of catecholamines on excitation-contraction coupling in frog single twitch fiber. Jpn J Physiol. 1977;27(2):195–213. doi: 10.2170/jjphysiol.27.195. [DOI] [PubMed] [Google Scholar]
  29. RALL T. W., SUTHERLAND E. W. Formation of a cyclic adenine ribonucleotide by tissue particles. J Biol Chem. 1958 Jun;232(2):1065–1076. [PubMed] [Google Scholar]
  30. Reuter H. Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature. 1983 Feb 17;301(5901):569–574. doi: 10.1038/301569a0. [DOI] [PubMed] [Google Scholar]
  31. Reuter H., Scholz H. The regulation of the calcium conductance of cardiac muscle by adrenaline. J Physiol. 1977 Jan;264(1):49–62. doi: 10.1113/jphysiol.1977.sp011657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanchez J. A., Stefani E. Inward calcium current in twitch muscle fibres of the frog. J Physiol. 1978 Oct;283:197–209. doi: 10.1113/jphysiol.1978.sp012496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schmid A., Renaud J. F., Lazdunski M. Short term and long term effects of beta-adrenergic effectors and cyclic AMP on nitrendipine-sensitive voltage-dependent Ca2+ channels of skeletal muscle. J Biol Chem. 1985 Oct 25;260(24):13041–13046. [PubMed] [Google Scholar]
  34. Siri L. N., Sánchez J. A., Stefani E. Effect of glycerol treatment on the calcium current of frog skeletal muscle. J Physiol. 1980 Aug;305:87–96. doi: 10.1113/jphysiol.1980.sp013351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stanfield P. R. A calcium dependent inward current in frog skeletal muscle fibres. Pflugers Arch. 1977 Apr 25;368(3):267–270. doi: 10.1007/BF00585206. [DOI] [PubMed] [Google Scholar]
  36. Sánchez J. A., Stefani E. Kinetic properties of calcium channels of twitch muscle fibres of the frog. J Physiol. 1983 Apr;337:1–17. doi: 10.1113/jphysiol.1983.sp014607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tsien R. W. Calcium channels in excitable cell membranes. Annu Rev Physiol. 1983;45:341–358. doi: 10.1146/annurev.ph.45.030183.002013. [DOI] [PubMed] [Google Scholar]
  38. Tsien R. W. Cyclic AMP and contractile activity in heart. Adv Cyclic Nucleotide Res. 1977;8:363–420. [PubMed] [Google Scholar]

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