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. 1985 Mar 1;85(3):383–408. doi: 10.1085/jgp.85.3.383

Calcium influx in contracting and paralyzed frog twitch muscle fibers

PMCID: PMC2215793  PMID: 3872927

Abstract

Calcium uptake produced by a potassium contracture in isolated frog twitch fibers was 6.7 +/- 0.8 pmol in 0.7 cm of fiber (mean +/- SEM, 21 observations) in the presence of 30 microM D600. When potassium was applied to fibers paralyzed by the combination of 30 microM D600, cold, and a prior contracture, the calcium uptake fell to 3.0 +/- 0.7 pmol (11): the fibers were soaked in 45Ca in sodium Ringer for 3 min before 45Ca, in a potassium solution, was added for 2 min; each estimate of uptake was corrected for 5 min of resting influx, measured from the same fiber (average = 2.3 +/- 0.3 pmol). The calcium influx into paralyzed fibers is unrelated to contraction. This voltage-sensitive, slowly inactivating influx, which can be blocked by 4 mM nickel, has properties similar to the calcium current described by several laboratories. The paired difference in calcium uptake between contracting and paralyzed fibers, 2.9 +/- 0.8 pmol (16), is a component of influx related to contraction. Its size varies with contracture size and it occurs after tension production: 45Ca applied immediately after contracture is taken up in essentially the same amounts as 45Ca added before contraction. This delayed uptake is probably a "reflux" refilling a binding site on the cytoplasmic side of the T membrane, which had been emptied during the prior contracture, perhaps to initiate it. We detect no component of calcium uptake related to excitation-contraction coupling occurring before or during a contracture.

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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. 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]
  3. 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]
  4. 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]
  5. Bianchi C. P. Some historical aspects of excitation--contraction coupling. Can J Physiol Pharmacol. 1982 Apr;60(4):415–416. doi: 10.1139/y82-061. [DOI] [PubMed] [Google Scholar]
  6. Blinks J. R., Olson C. B., Jewell B. R., Bravený P. Influence of caffeine and other methylxanthines on mechanical properties of isolated mammalian heart muscle. Evidence for a dual mechanism of action. Circ Res. 1972 Apr;30(4):367–392. doi: 10.1161/01.res.30.4.367. [DOI] [PubMed] [Google Scholar]
  7. Burnstock G. Purinergic nerves. Pharmacol Rev. 1972 Sep;24(3):509–581. [PubMed] [Google Scholar]
  8. Burnstock G. Purinergic receptors. J Theor Biol. 1976 Oct 21;62(2):491–503. doi: 10.1016/0022-5193(76)90133-8. [DOI] [PubMed] [Google Scholar]
  9. CURTIS B. A. Some effects of Ca-free choline-Ringer solution on frog skeletal muscle. J Physiol. 1963 Apr;166:75–86. doi: 10.1113/jphysiol.1963.sp007091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Caputo C. Nickel substitution for calcium and the time course of potassium contractures of single muscle fibres. J Muscle Res Cell Motil. 1981 Jun;2(2):167–182. doi: 10.1007/BF00711867. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Changeux J. P., Kasai M., Lee C. Y. Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1241–1247. doi: 10.1073/pnas.67.3.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Curtis B. A. Ca fluxes in single twitch muscle fibers. J Gen Physiol. 1966 Nov;50(2):255–267. doi: 10.1085/jgp.50.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Curtis B. A. Calcium efflux from frog twitch muscle fibers. J Gen Physiol. 1970 Feb;55(2):243–253. [PubMed] [Google Scholar]
  15. 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]
  16. Donaldson P. L., Beam K. G. Calcium currents in a fast-twitch skeletal muscle of the rat. J Gen Physiol. 1983 Oct;82(4):449–468. doi: 10.1085/jgp.82.4.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Eisenberg B. R., Eisenberg R. S. The T-SR junction in contracting single skeletal muscle fibers. J Gen Physiol. 1982 Jan;79(1):1–19. doi: 10.1085/jgp.79.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Eisenberg R. S., Mathias R. T., Rae J. S. Measurement, modeling, and analysis of the linear electrical properties of cells. Ann N Y Acad Sci. 1977 Dec 30;303:342–354. [PubMed] [Google Scholar]
  19. Eisenberg R. S., McCarthy R. T., Milton R. L. Paralysis of frog skeletal muscle fibres by the calcium antagonist D-600. J Physiol. 1983 Aug;341:495–505. doi: 10.1113/jphysiol.1983.sp014819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Elliott G. F. Donnan and osmotic effects in muscle fibres without membranes. J Mechanochem Cell Motil. 1973 May;2(1):83–89. [PubMed] [Google Scholar]
  21. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol. 1983 Jul;245(1):C1–14. doi: 10.1152/ajpcell.1983.245.1.C1. [DOI] [PubMed] [Google Scholar]
  22. Fischman D. A., Swan R. C. Nickel substitution for calcium in excitation-contraction coupling of skeletal muscle. J Gen Physiol. 1967 Jul;50(6):1709–1728. doi: 10.1085/jgp.50.6.1709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fosset M., Jaimovich E., Delpont E., Lazdunski M. [3H]nitrendipine labelling of the Ca2+ channel in skeletal muscle. Eur J Pharmacol. 1982 Dec 17;86(1):141–142. doi: 10.1016/0014-2999(82)90414-9. [DOI] [PubMed] [Google Scholar]
  24. Fosset M., Jaimovich E., Delpont E., Lazdunski M. [3H]nitrendipine receptors in skeletal muscle. J Biol Chem. 1983 May 25;258(10):6086–6092. [PubMed] [Google Scholar]
  25. Franzini-Armstrong C. Membrane particles and transmission at the triad. Fed Proc. 1975 Apr;34(5):1382–1389. [PubMed] [Google Scholar]
  26. Franzini-Armstrong C., Nunzi G. Junctional feet and particles in the triads of a fast-twitch muscle fibre. J Muscle Res Cell Motil. 1983 Apr;4(2):233–252. doi: 10.1007/BF00712033. [DOI] [PubMed] [Google Scholar]
  27. Gonzalez-Serratos H., Valle-Aguilera R., Lathrop D. A., Garcia M. C. Slow inward calcium currents have no obvious role in muscle excitation-contraction coupling. Nature. 1982 Jul 15;298(5871):292–294. doi: 10.1038/298292a0. [DOI] [PubMed] [Google Scholar]
  28. Gordon A. M., Huxley A. F., Julian F. J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192. doi: 10.1113/jphysiol.1966.sp007909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Graf F., Schatzmann H. J. Some effects of removal of external calcium on pig striated muscle. J Physiol. 1984 Apr;349:1–13. doi: 10.1113/jphysiol.1984.sp015138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. HILL A. V. The abrupt transition from rest to activity in muscle. Proc R Soc Lond B Biol Sci. 1949 Oct;136(884):399–420. doi: 10.1098/rspb.1949.0033. [DOI] [PubMed] [Google Scholar]
  31. HODGKIN A. L., HOROWICZ P. Movements of Na and K in single muscle fibres. J Physiol. 1959 Mar 3;145(2):405–432. doi: 10.1113/jphysiol.1959.sp006150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. HODGKIN A. L., KEYNES R. D. Movements of labelled calcium in squid giant axons. J Physiol. 1957 Sep 30;138(2):253–281. doi: 10.1113/jphysiol.1957.sp005850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Henon B. K., McAfee D. A. The ionic basis of adenosine receptor actions on post-ganglionic neurones in the rat. J Physiol. 1983 Mar;336:607–620. doi: 10.1113/jphysiol.1983.sp014600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hui C. S., Milton R. L., Eisenberg R. S. Charge movement in skeletal muscle fibers paralyzed by the calcium-entry blocker D600. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2582–2585. doi: 10.1073/pnas.81.8.2582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. KEYNES R. D. The ionic movements during nervous activity. J Physiol. 1951 Jun;114(1-2):119–150. doi: 10.1113/jphysiol.1951.sp004608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kirsch G. E., Nichols R. A., Nakajima S. Delayed rectification in the transverse tubules: origin of the late after-potential in frog skeletal muscle. J Gen Physiol. 1977 Jul;70(1):1–21. doi: 10.1085/jgp.70.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Latorre R., Vergara C., Hidalgo C. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci U S A. 1982 Feb;79(3):805–809. doi: 10.1073/pnas.79.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lau Y. H., Caswell A. H., Brunschwig J. P. Isolation of transverse tubules by fractionation of triad junctions of skeletal muscle. J Biol Chem. 1977 Aug 10;252(15):5565–5574. [PubMed] [Google Scholar]
  41. 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]
  42. Magleby K. L., Pallotta B. S. Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:585–604. doi: 10.1113/jphysiol.1983.sp014957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Matsubara I., Elliott G. F. X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J Mol Biol. 1972 Dec 30;72(3):657–669. doi: 10.1016/0022-2836(72)90183-0. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Mitchell R. D., Saito A., Palade P., Fleischer S. Morphology of isolated triads. J Cell Biol. 1983 Apr;96(4):1017–1029. doi: 10.1083/jcb.96.4.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. NARAHASHI T., MOORE J. W., SCOTT W. R. TETRODOTOXIN BLOCKAGE OF SODIUM CONDUCTANCE INCREASE IN LOBSTER GIANT AXONS. J Gen Physiol. 1964 May;47:965–974. doi: 10.1085/jgp.47.5.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. NIEDERGERKE R. Movements of Ca in beating ventricles of the frog heart. J Physiol. 1963 Jul;167:551–580. doi: 10.1113/jphysiol.1963.sp007167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Rosemblatt M., Hidalgo C., Vergara C., Ikemoto N. Immunological and biochemical properties of transverse tubule membranes isolated from rabbit skeletal muscle. J Biol Chem. 1981 Aug 10;256(15):8140–8148. [PubMed] [Google Scholar]
  50. Sandow A. Excitation-contraction coupling in skeletal muscle. Pharmacol Rev. 1965 Sep;17(3):265–320. [PubMed] [Google Scholar]
  51. 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]
  52. Schneider M. F. Membrane charge movement and depolarization-contraction coupling. Annu Rev Physiol. 1981;43:507–517. doi: 10.1146/annurev.ph.43.030181.002451. [DOI] [PubMed] [Google Scholar]
  53. Snyder S. H. Drug and neurotransmitter receptors in the brain. Science. 1984 Apr 6;224(4644):22–31. doi: 10.1126/science.6322304. [DOI] [PubMed] [Google Scholar]
  54. Somlyo A. V. Bridging structures spanning the junctioning gap at the triad of skeletal muscle. J Cell Biol. 1979 Mar;80(3):743–750. doi: 10.1083/jcb.80.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Stefani E., Chiarandini D. J. Ionic channels in skeletal muscle. Annu Rev Physiol. 1982;44:357–372. doi: 10.1146/annurev.ph.44.030182.002041. [DOI] [PubMed] [Google Scholar]
  56. Stephenson E. W. Activation of fast skeletal muscle: contributions of studies on skinned fibers. Am J Physiol. 1981 Jan;240(1):C1–19. doi: 10.1152/ajpcell.1981.240.1.C1. [DOI] [PubMed] [Google Scholar]

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