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. 1985 Jul;48(1):33–45. doi: 10.1016/S0006-3495(85)83758-9

Extracellular calcium ion depletion in frog cardiac ventricular muscle.

K P Dresdner, R P Kline
PMCID: PMC1329375  PMID: 3874655

Abstract

The extracellular free [Ca++] in frog ventricular muscle strips was monitored using single-barrel calcium ion-selective microelectrodes. During trains of repetitive stimulation, a heart rate-dependent, sustained fall (depletion) of the extracellular free [Ca++] occurs, which is most likely a consequence of net Ca++ influx into ventricular cells. The magnitude of the [Ca++]0 depletion increases for higher Ringer's solution [Ca++], and is reversibly blocked by manganese ion. Prolonged repetitive field stimulation (20-30 min) activates additional cellular Ca++ efflux, which can balance the additional Ca++ influx caused by stimulation, resulting in abolition of extratrabecular [Ca++]0 depletion in 20-30 min, and hence zero net transmembrane Ca++ flux at steady state. In the poststimulation period of quiescence, cellular Ca++ efflux persists and causes an elevation (accumulation) of the extracellular free [Ca++]. From these [Ca++]0 depletions, quantitative estimates for the net transmembrane Ca++ flux were derived using an analytical solution to the diffusion equation. In the highest Ringer's solution [Ca++] used (1 mM) the calculated net increase of the total intracellular calcium per beat was 6.5 +/- 1.4 mumol/l of intracellular space. This corresponds to an average net transmembrane Ca++ influx of 0.81 +/- 0.17 pmol/cm2/s during the 800-ms action potential. In lower bath [Ca++] the net transmembrane [Ca++] flux was proportionately reduced.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen D. G., Blinks J. R. Calcium transients in aequorin-injected frog cardiac muscle. Nature. 1978 Jun 15;273(5663):509–513. doi: 10.1038/273509a0. [DOI] [PubMed] [Google Scholar]
  2. Attwell D., Eisner D., Cohen I. Voltage clamp and tracer flux data: effects of a restricted extra-cellular space. Q Rev Biophys. 1979 Aug;12(3):213–261. doi: 10.1017/s0033583500005448. [DOI] [PubMed] [Google Scholar]
  3. Baker P. F. Transport and metabolism of calcium ions in nerve. Prog Biophys Mol Biol. 1972;24:177–223. doi: 10.1016/0079-6107(72)90007-7. [DOI] [PubMed] [Google Scholar]
  4. Bers D. M. Early transient depletion of extracellular Ca during individual cardiac muscle contractions. Am J Physiol. 1983 Mar;244(3):H462–H468. doi: 10.1152/ajpheart.1983.244.3.H462. [DOI] [PubMed] [Google Scholar]
  5. Brown A. M., Orkand R. K. A down then up staircase in frog ventricle due to altered excitation-contraction coupling. J Physiol. 1968 Jul;197(2):295–304. doi: 10.1113/jphysiol.1968.sp008560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caroni P., Carafoli E. The Ca2+-pumping ATPase of heart sarcolemma. Characterization, calmodulin dependence, and partial purification. J Biol Chem. 1981 Apr 10;256(7):3263–3270. [PubMed] [Google Scholar]
  7. Chapman R. A., Ellis D. The effects of manganese ions on the contraction of the frog's heart. J Physiol. 1977 Nov;272(2):331–354. doi: 10.1113/jphysiol.1977.sp012047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chapman R. A. Excitation-contraction coupling in cardiac muscle. Prog Biophys Mol Biol. 1979;35(1):1–52. doi: 10.1016/0079-6107(80)90002-4. [DOI] [PubMed] [Google Scholar]
  9. Cohen I., Kline R. K+ fluctuations in the extracellular spaces of cardiac muscle. Evidence from the voltage clamp and extracellular K+ - selective microelectrodes. Circ Res. 1982 Jan;50(1):1–16. [PubMed] [Google Scholar]
  10. Dagostino M., Lee C. O. Neutral carrier Na+- and Ca2+-selective microelectrodes for intracellular application. Biophys J. 1982 Dec;40(3):199–207. doi: 10.1016/S0006-3495(82)84475-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fabiato A., Fabiato F. Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat, and frog hearts and from fetal and new-born rat ventricles. Ann N Y Acad Sci. 1978 Apr 28;307:491–522. doi: 10.1111/j.1749-6632.1978.tb41979.x. [DOI] [PubMed] [Google Scholar]
  12. Hilgemann D. W., Delay M. J., Langer G. A. Activation-dependent cumulative depletions of extracellular free calcium in guinea pig atrium measured with antipyrylazo III and tetramethylmurexide. Circ Res. 1983 Dec;53(6):779–793. doi: 10.1161/01.res.53.6.779. [DOI] [PubMed] [Google Scholar]
  13. Hilgemann D. W., Langer G. A. Transsarcolemmal calcium movements in arterially perfused rabbit right ventricle measured with extracellular calcium-sensitive dyes. Circ Res. 1984 Apr;54(4):461–467. doi: 10.1161/01.res.54.4.461. [DOI] [PubMed] [Google Scholar]
  14. Hume J. R., Giles W. Ionic currents in single isolated bullfrog atrial cells. J Gen Physiol. 1983 Feb;81(2):153–194. doi: 10.1085/jgp.81.2.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kline R. P., Kupersmith J. Effects of extracellular potassium accumulation and sodium pump activation on automatic canine Purkinje fibres. J Physiol. 1982 Mar;324:507–533. doi: 10.1113/jphysiol.1982.sp014127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kline R. P., Morad M. Potassium efflux in heart muscle during activity: extracellular accumulation and its implications. J Physiol. 1978 Jul;280:537–558. doi: 10.1113/jphysiol.1978.sp012400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kline R., Morad M. Potassium efflux and accumulation in heart muscle. Evidence from K +/- electrode experiments. Biophys J. 1976 Apr;16(4):367–372. doi: 10.1016/S0006-3495(76)85694-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kunze D. L. Rate-dependent changes in extracellular potassium in the rabbit atrium. Circ Res. 1977 Jul;41(1):122–127. doi: 10.1161/01.res.41.1.122. [DOI] [PubMed] [Google Scholar]
  19. Lee C. O. Ionic activities in cardiac muscle cells and application of ion-selective microelectrodes. Am J Physiol. 1981 Oct;241(4):H459–H478. doi: 10.1152/ajpheart.1981.241.4.H459. [DOI] [PubMed] [Google Scholar]
  20. Lee C. O., Uhm D. Y., Dresdner K. Sodium-calcium exchange in rabbit heart muscle cells: direct measurement of sarcoplasmic Ca2+ activity. Science. 1980 Aug 8;209(4457):699–701. doi: 10.1126/science.7394527. [DOI] [PubMed] [Google Scholar]
  21. Martin G., Morad M. Activity-induced potassium accumulation and its uptake in frog ventricular muscle. J Physiol. 1982 Jul;328:205–227. doi: 10.1113/jphysiol.1982.sp014260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Morad M., Orkand R. K. Excitation-concentration coupling in frog ventricle: evidence from voltage clamp studies. J Physiol. 1971 Dec;219(1):167–189. doi: 10.1113/jphysiol.1971.sp009656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mullins L. J. A mechanism for Na/Ca transport. J Gen Physiol. 1977 Dec;70(6):681–695. doi: 10.1085/jgp.70.6.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Niedergerke R., Orkand R. K. The dual effect of calcium on the action potential of the frog's heart. J Physiol. 1966 May;184(2):291–311. doi: 10.1113/jphysiol.1966.sp007916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Niedergerke R., Page S., Talbot M. S. Calcium fluxes in frog heart ventricles. Pflugers Arch. 1969;306(4):357–360. doi: 10.1007/BF00589161. [DOI] [PubMed] [Google Scholar]
  27. Page S. G., Niedergerke R. Structures of physiological interest in the frog heart ventricle. J Cell Sci. 1972 Jul;11(1):179–203. doi: 10.1242/jcs.11.1.179. [DOI] [PubMed] [Google Scholar]
  28. 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. Pflugers Arch. 1969;308(2):91–110. doi: 10.1007/BF00587018. [DOI] [PubMed] [Google Scholar]
  29. Tsien R. Y., Rink T. J. Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim Biophys Acta. 1980 Jul;599(2):623–638. doi: 10.1016/0005-2736(80)90205-9. [DOI] [PubMed] [Google Scholar]

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