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. 1988 Nov;405:233–255. doi: 10.1113/jphysiol.1988.sp017331

Mechanism of release of calcium from sarcoplasmic reticulum of guinea-pig cardiac cells.

D J Beuckelmann 1, W G Wier 1
PMCID: PMC1190974  PMID: 2475607

Abstract

1. The mechanisms that control release of Ca2+ from the sarcoplasmic reticulum (SR) of guinea-pig ventricular cells were studied by observing intracellular calcium concentration ([Ca2+]i transients) and membrane currents in voltage-clamped guinea-pig ventricular myocytes perfused internally with Fura-2. 2. Sarcolemmal Ca2+ current was identified through the use of tetrodotoxin (TTX) and Ca2+ channel antagonists (verapamil) and agonists (Bay K 8644). 3. Changes in [Ca2+]i attributable to release of Ca2+ from the SR were identified through the use of ryanodine, which abolishes the ability of the SR to release Ca2+. Ryanodine-sensitive increases in [Ca2+]i could be elicited either by depolarization or by repolarization (from depolarizing pulses to relatively positive membrane potentials). 4. At appropriate voltages, it is the initial fast change in [Ca2+]i elicited by either depolarization or repolarization that is abolished by ryanodine, and is defined here as ryanodine sensitive. 5. The amplitude of the ryanodine-sensitive [Ca2+]i transient elicited by depolarization had a bell-shaped dependence on membrane potential with a maximum of about 500 nM at 10 mV, and with the upper minimum between 60 and 70 mV. Verapamil-sensitive current activated over approximately the same potential range as the [Ca2+]i transient, with a peak amplitude at 10 mV, and a reversal potential of 65 mV. 6. When a holding potential of -68 mV and TTX (30 microM) were used, the most negative pulse potential at which activation of an inward current occurred was -49 mV while changes in [Ca2+]i occurred at -43 mV. 7. Ryanodine-sensitive increases in [Ca2+]i elicited by repolarization (tail transients) were maximal for repolarization to 0 mV. Smaller changes in [Ca2+]i than maximal were elicited by repolarization to both more positive and more negative potentials than 0 mV. The peak amplitude of the verapamil-sensitive tail currents elicited by repolarization increased continuously as the membrane was repolarized to potentials more negative than 60 mV. 8. Increasing depolarizing pulse duration beyond 10-20 ms did not increase the amplitude of the [Ca2+]i transient, but prolonged it. 9. The experimental results are compared to the predictions of two theories on the mechanism of excitation-contraction coupling: Ca2+-induced release of Ca2+ (CICR), as it has been formulated from data in skinned cardiac cells, and a charge-coupled release mechanism (CCRM), as it has been formulated to explain excitation-contraction coupling in skeletal muscle. 10. Some of the results are clearly not consistent with certain features of a charge-coupled release mechanism.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Adrian R. H., Chandler W. K., Hodgkin A. L. The kinetics of mechanical activation in frog muscle. J Physiol. 1969 Sep;204(1):207–230. doi: 10.1113/jphysiol.1969.sp008909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barcenas-Ruiz L., Beuckelmann D. J., Wier W. G. Sodium-calcium exchange in heart: membrane currents and changes in [Ca2+]i. Science. 1987 Dec 18;238(4834):1720–1722. doi: 10.1126/science.3686010. [DOI] [PubMed] [Google Scholar]
  3. Barcenas-Ruiz L., Wier W. G. Voltage dependence of intracellular [Ca2+]i transients in guinea pig ventricular myocytes. Circ Res. 1987 Jul;61(1):148–154. doi: 10.1161/01.res.61.1.148. [DOI] [PubMed] [Google Scholar]
  4. Baylor S. M., Chandler W. K., Marshall M. W. Calcium release and sarcoplasmic reticulum membrane potential in frog skeletal muscle fibres. J Physiol. 1984 Mar;348:209–238. doi: 10.1113/jphysiol.1984.sp015106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylor S. M., Chandler W. K., Marshall M. W. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol. 1983 Nov;344:625–666. doi: 10.1113/jphysiol.1983.sp014959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brum G., Stefani E., Rios E. Simultaneous measurements of Ca2+ currents and intracellular Ca2+ concentrations in single skeletal muscle fibers of the frog. Can J Physiol Pharmacol. 1987 Apr;65(4):681–685. doi: 10.1139/y87-112. [DOI] [PubMed] [Google Scholar]
  7. Cannell M. B., Berlin J. R., Lederer W. J. Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science. 1987 Dec 4;238(4832):1419–1423. doi: 10.1126/science.2446391. [DOI] [PubMed] [Google Scholar]
  8. Chandler W. K., Rakowski R. F., Schneider M. F. Effects of glycerol treatment and maintained depolarization on charge movement in skeletal muscle. J Physiol. 1976 Jan;254(2):285–316. doi: 10.1113/jphysiol.1976.sp011233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fabiato A. Rapid ionic modifications during the aequorin-detected calcium transient in a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):189–246. doi: 10.1085/jgp.85.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fabiato A. Simulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):291–320. doi: 10.1085/jgp.85.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):247–289. doi: 10.1085/jgp.85.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fleischer S., Ogunbunmi E. M., Dixon M. C., Fleer E. A. Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7256–7259. doi: 10.1073/pnas.82.21.7256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  14. Hadley R. W., Hume J. R. An intrinsic potential-dependent inactivation mechanism associated with calcium channels in guinea-pig myocytes. J Physiol. 1987 Aug;389:205–222. doi: 10.1113/jphysiol.1987.sp016654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hess P., Lansman J. B., Tsien R. W. Calcium channel selectivity for divalent and monovalent cations. Voltage and concentration dependence of single channel current in ventricular heart cells. J Gen Physiol. 1986 Sep;88(3):293–319. doi: 10.1085/jgp.88.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hess P., Lansman J. B., Tsien R. W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984 Oct 11;311(5986):538–544. doi: 10.1038/311538a0. [DOI] [PubMed] [Google Scholar]
  17. Inui M., Saito A., Fleischer S. Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J Biol Chem. 1987 Nov 15;262(32):15637–15642. [PubMed] [Google Scholar]
  18. Inui M., Saito A., Fleischer S. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem. 1987 Feb 5;262(4):1740–1747. [PubMed] [Google Scholar]
  19. Kimura J., Miyamae S., Noma A. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol. 1987 Mar;384:199–222. doi: 10.1113/jphysiol.1987.sp016450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kovács L., Ríos E., Schneider M. F. Calcium transients and intramembrane charge movement in skeletal muscle fibres. Nature. 1979 May 31;279(5712):391–396. doi: 10.1038/279391a0. [DOI] [PubMed] [Google Scholar]
  21. Lai F. A., Erickson H. P., Rousseau E., Liu Q. Y., Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature. 1988 Jan 28;331(6154):315–319. doi: 10.1038/331315a0. [DOI] [PubMed] [Google Scholar]
  22. Lee K. S., Marban E., Tsien R. W. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium. J Physiol. 1985 Jul;364:395–411. doi: 10.1113/jphysiol.1985.sp015752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee K. S., Tsien R. W. Reversal of current through calcium channels in dialysed single heart cells. Nature. 1982 Jun 10;297(5866):498–501. doi: 10.1038/297498a0. [DOI] [PubMed] [Google Scholar]
  24. London B., Krueger J. W. Contraction in voltage-clamped, internally perfused single heart cells. J Gen Physiol. 1986 Oct;88(4):475–505. doi: 10.1085/jgp.88.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marban E., Wier W. G. Ryanodine as a tool to determine the contributions of calcium entry and calcium release to the calcium transient and contraction of cardiac Purkinje fibers. Circ Res. 1985 Jan;56(1):133–138. doi: 10.1161/01.res.56.1.133. [DOI] [PubMed] [Google Scholar]
  26. Matsuda H., Noma A. Isolation of calcium current and its sensitivity to monovalent cations in dialysed ventricular cells of guinea-pig. J Physiol. 1984 Dec;357:553–573. doi: 10.1113/jphysiol.1984.sp015517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Meissner G., Darling E., Eveleth J. Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides. Biochemistry. 1986 Jan 14;25(1):236–244. doi: 10.1021/bi00349a033. [DOI] [PubMed] [Google Scholar]
  28. Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem. 1986 May 15;261(14):6300–6306. [PubMed] [Google Scholar]
  29. Melzer W., Rios E., Schneider M. F. Time course of calcium release and removal in skeletal muscle fibers. Biophys J. 1984 Mar;45(3):637–641. doi: 10.1016/S0006-3495(84)84203-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Melzer W., Ríos E., Schneider M. F. The removal of myoplasmic free calcium following calcium release in frog skeletal muscle. J Physiol. 1986 Mar;372:261–292. doi: 10.1113/jphysiol.1986.sp016008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Melzer W., Schneider M. F., Simon B. J., Szucs G. Intramembrane charge movement and calcium release in frog skeletal muscle. J Physiol. 1986 Apr;373:481–511. doi: 10.1113/jphysiol.1986.sp016059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Miledi R., Parker I., Zhu P. H. Calcium transients studied under voltage-clamp control in frog twitch muscle fibres. J Physiol. 1983 Jul;340:649–680. doi: 10.1113/jphysiol.1983.sp014785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mitchell M. R., Powell T., Terrar D. A., Twist V. W. Ryanodine prolongs Ca-currents while suppressing contraction in rat ventricular muscle cells. Br J Pharmacol. 1984 Jan;81(1):13–15. doi: 10.1111/j.1476-5381.1984.tb10735.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Philipson K. D. Sodium-calcium exchange in plasma membrane vesicles. Annu Rev Physiol. 1985;47:561–571. doi: 10.1146/annurev.ph.47.030185.003021. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Sanguinetti M. C., Krafte D. S., Kass R. S. Voltage-dependent modulation of Ca channel current in heart cells by Bay K8644. J Gen Physiol. 1986 Sep;88(3):369–392. doi: 10.1085/jgp.88.3.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schramm M., Thomas G., Towart R., Franckowiak G. Novel dihydropyridines with positive inotropic action through activation of Ca2+ channels. Nature. 1983 Jun 9;303(5917):535–537. doi: 10.1038/303535a0. [DOI] [PubMed] [Google Scholar]
  38. Volpe P., Stephenson E. W. Ca2+ dependence of transverse tubule-mediated calcium release in skinned skeletal muscle fibers. J Gen Physiol. 1986 Feb;87(2):271–288. doi: 10.1085/jgp.87.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wier W. G., Cannell M. B., Berlin J. R., Marban E., Lederer W. J. Cellular and subcellular heterogeneity of [Ca2+]i in single heart cells revealed by fura-2. Science. 1987 Jan 16;235(4786):325–328. doi: 10.1126/science.3798114. [DOI] [PubMed] [Google Scholar]
  40. Wier W. G., Yue D. T. Intracellular calcium transients underlying the short-term force-interval relationship in ferret ventricular myocardium. J Physiol. 1986 Jul;376:507–530. doi: 10.1113/jphysiol.1986.sp016167. [DOI] [PMC free article] [PubMed] [Google Scholar]

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