Pflügers Archiv

, Volume 379, Issue 3, pp 259–268 | Cite as

The dependence of twitch relaxation on sodium ions and on internal Ca2+ stores in voltage clamped frog atrial fibres

  • Marie-Jeanne Roulet
  • K. G. Mongo
  • G. Vassort
  • Renée Ventura-Clapier
Excitable Tissues and Central Nervous Physiology
Received:

Abstract

Frog heart relaxation was analyzed under voltage clamp conditions as the tension decay observed after the membrane potential had been returned to its resting value. The tension decayed exponentially with a time constant of 188±3.8 ms SEM. The relaxation rate decreased with the external Na concentration. It fell to about one tenth in a Na-free solution. Increasing the intracellular Na-content by an application of veratrine also decreased the relaxation rate. Thus relaxation seems dependent on the Na gradient. The relaxation rate decreased within one second upon switching from a high to a low Na-containing solution. The relaxation rate reached a minimum before rising slightly to a new steady state value. This rebound may reflect the partial recovery of the Na gradient since a fast variation in [Na]i follows alteration of [Na]o. Mn and La ions also slowed relaxation. In a Na-free solution, adrenaline accelerated tension decay, an effect not noticeable in frog heart contained in Ringer solution. Other cAMP-promoting agents, such as dibutyryl-cAMP and aminophylline, also increased relaxation rate.

It is concluded that in frog myocardium, part of the decrease of the intracellular Ca2+-concentration which occurs during each cardiac cycle could be dependent on a Na−Ca exchange mechanism. The relative importance of this mechanism, versus internal Ca sequestration, in the relaxation of tension may well be greater in contractile tissues whose cells have a large surface/volume ratio.

Key words

Relaxation Na ions Na−Ca exchange Frog heart Cyclic AMP 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Beeler, G. W., Reuter, H.: Membrane calcium current in ventricular myocardial fibres. J. Physiol. (Lond.)207, 191–210 (1970a)Google Scholar
  2. Beeler, G. W., Reuter, H.: The relation between membrane potential, membrane currents and activation of contraction in ventricular myocardial fibres. J. Physiol. (Lond.)207, 211–230 (1970b)Google Scholar
  3. Benninger, C., Einwächter, H. M., Haas, H. G., Kern, R.: Calciumsodium antagonism on the frog's heart: a voltage clamp study. J. Physiol. (Lond.)259, 617–645 (1976)Google Scholar
  4. Blaustein, M. P.: The interrelationships between sodium and calcium fluxes across membranes. Rev. Physiol. Biol. Pharmacol.70, 33–82 (1974)Google Scholar
  5. Einwächter, H. M., Haas, H. G., Kern, R.: Membrane current and contraction in frog atrial fibres. J. Physiol. (Lond.)227, 141–171 (1972)Google Scholar
  6. Ellis, D.: The effects of external cations and ouabain on the intracellular sodium activity of sheep heart Purkinje fibres. J. Physiol. (Lond.)273, 211–240 (1977)Google Scholar
  7. Endo, M.: Calcium release from the sarcoplasmic reticulum. Physiol. Rev.57, 71–108 (1977)Google Scholar
  8. Fabiato, A., Fabiato, F.: Relaxing and inotropic effects of cAMP on skinned cardiac cells. Nature253, 556–558 (1975)Google Scholar
  9. Fleckenstein, A., Hertel, H.: Über die Zustandsänderung des kontraktilen Systems in Abhängigkeit vom extracellulären Kalium und Natrium. Pflügers Arch. ges. Physiol.250, 577–597 (1948)Google Scholar
  10. Glitsch, H. G., Reuter, H., Scholz, H.: The effect of the internal concentration on calcium fluxes in isolated guinea-pig auricles. J. Physiol. (Lond.)209, 25–43 (1970)Google Scholar
  11. Goto, M., Kimoto, Y., Suetsugu, Y.: Membrane currents responsible for contraction and relaxation of the bullfrog ventricle. Jap. J. Physiol.22, 315–331 (1972a)Google Scholar
  12. Goto, M., Kimoto, Y., Saito, M., Wada Y.: Tension fall after contraction of bullfrog atria muscle examined with the voltage clamp technique. Jap. J. Physiol.22, 637–650 (1972b)Google Scholar
  13. Horackova, M., Vassort, G.: Excitation-contraction coupling in frog heart. Effect of veratrine. Pflügers Arch.352, 291–302 (1974)Google Scholar
  14. Horackova, M., Vassort, G.: Na−Ca exchange in regulation of cardiac contractility: evidence for electrogenic, voltagedependent mechanism. J. Gen. Physiol. (in press, 1979)Google Scholar
  15. Jewell, B. R., Wilkie, D. R.: The mechanical properties of relaxing muscle. J. Physiol. (Lond.)152, 30–47 (1960)Google Scholar
  16. Julian, F. J., Moss, R. L.: Brief Reviews: The concept of active state in striated muscle. Circ. Res.38, 53–59 (1976)Google Scholar
  17. Jundt, H., Porzig, H., Reuter, H., Stucki, J. W.: The effects of substances releasing intracellular calcium ions on sodium dependent calcium efflux from guinea-pig auricles. J. Physiol. (Lond.)246, 229–253 (1975)Google Scholar
  18. Keenan, M. J., Niedergerke, R.: Intracellular sodium concentration and resting sodium fluxes of the frog heart ventricle. J. Physiol. (Lond.)188, 235–260 (1967)Google Scholar
  19. Langer, G. A.: Heart: excitation-contraction coupling. Ann. Rev. Physiol.35, 55–86 (1973)Google Scholar
  20. La Raia, P. J., Morkin, E.: Adenosine 3′,5′-monophosphate-dependent membrane phosphorylation. A possible mechanism for the control of microsomal calcium transport in heart muscle. Circ. Res.35, 298–306 (1974)Google Scholar
  21. Lüttgau, H. C., Niedergerke, R.: The antagonism between Ca and Na ions on the frog's heart. J. Physiol. (Lond.)143, 486–505 (1958)Google Scholar
  22. Meinertz, T., Nawrath, H., Scholz, H.: Relaxant effects of dibutyryl cyclic AMP on mammalian cardiac muscle. J. Cyclic Nucl. Res.1, 31–36 (1975)Google Scholar
  23. Miller, D. J., Moisescu, D. G.: The effects of very low external calcium and sodium concentrations on cardiac contractile strength and calcium-sodium antagonism. J. Physiol. (Lond.)259, 283–308 (1976)Google Scholar
  24. Mobley, B. A., Page, E.: The surface area of sheep cardiac Purkinje fibres. J. Physiol. (Lond.).220, 547–563 (1972)Google Scholar
  25. Morad, M., Rolett, E. L.: Relaxing effects of catecholamines on mammalian heart. J. Physiol. (Lond.)224, 537–558 (1972)Google Scholar
  26. Niedergerke, R.: Movements of Ca in beating ventricles of the frog heart. J. Physiol. (Lond.)167, 551–580 (1963)Google Scholar
  27. Niedergerke, R., Page, S., Talbot, M. S.: Calcium fluxes in frog ventricles. Pflügers Arch.306, 357–360 (1969)Google Scholar
  28. Page, S. G., Niedergerke, R.: Structures of physiological interest in the frog heart ventricle. J. Cell. Sci.11, 179–203 (1972)Google Scholar
  29. Page, E., McAllister, L. P., Power, B.: Sterological measurements of cardiac ultrastructures implicated in excitation contraction coupling. (sarcotubules and T-system). Proc. Natl. Acad. Sci. USA68, 1465–1466 (1971)Google Scholar
  30. Parmley, W. W., Sonnenblick, E. H.: Relation between mechanics of contraction and relaxation in mammalian cardiac muscle. Am. J. Physiol.216, 1084–1091 (1969)Google Scholar
  31. Reiter, M.: Differences in the inotropic cardiac effects of noradrenaline and dihydro-ouabain. Naunyn-Schmiedeberg's Arch. Pharmacol.275, 243–250 (1972)Google Scholar
  32. Reuter, H., Seitz, N.: The dependence of calcium efflux from cardiac muscle on temperature and external ion composition. J. Physiol. (Lond.)195, 451–470 (1968)Google Scholar
  33. Rougier, O., Vassort, G., Garnier, D., Gargouil, Y. M., Coraboeuf, E.: Existence and role of a slow inward current during the frog atrial action potential. Pflügers Arch.308, 91–110 (1969)Google Scholar
  34. Russell, J. M., Blaustein, M. P.: Calcium efflux from barnacle muscle fibers. Dependence on external cations. J. Gen. Physiol.63, 144–167 (1974)Google Scholar
  35. Scarpa, A., Graziotti, P.: Mechanisms for intracellular calcium regulation in heart. 1. Stopped-flow measurements of Ca2+ uptake by cardiac mitochondria. J. Gen. Physiol.62, 756–772 (1973)Google Scholar
  36. Tsien, R. W.: Cyclic AMP and contractile activity in heart. Adv. Cyclic Nucl. Res.8, 363–420 (1977)Google Scholar
  37. Van Breemen, C., De Weer, P.: Lanthanum inhibition of45Ca efflux from the squid giant axon. Nature226, 760–761 (1970)Google Scholar
  38. Vassort, G.: Influence of sodium on the regulation of frog myocardial contractility. Pflügers Arch.339, 225–240 (1973)Google Scholar
  39. Vassort, G., Rougier, O.: Membrane potential and slow inward current dependence of frog cardiac mechanical activity. Pflügers Arch.331, 191–203 (1972)Google Scholar
  40. Verdonck, F., Carmeliet, E.: Isometric contractions in cardiac Purkinje fibres: characteristics in Na-free Sr tyrode. Cardiovas. Res. suppl.1, 76–83 (1971)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • Marie-Jeanne Roulet
    • 1
  • K. G. Mongo
    • 1
  • G. Vassort
    • 1
  • Renée Ventura-Clapier
    • 1
  1. 1.Laboratoire de Physiologie Comparée et de Physiologie Cellulaire associé au CNRSUniversité Paris-SudOrsayFrance

Personalised recommendations