Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1985 Feb 1;85(2):247–289. doi: 10.1085/jgp.85.2.247

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

PMCID: PMC2215800  PMID: 2580043

Abstract

Microprocessor-controlled changes of [free Ca2+] at the outer surface of the sarcoplasmic reticulum (SR) wrapped around individual myofibrils of a skinned canine cardiac Purkinje cell and aequorin bioluminescence recording were used to study the mechanism of Ca2+-induced release of Ca2+ from the SR. This Ca2+ release is triggered by a rapid increase of [free Ca2+] at the outer surface of the SR of a previously quiescent skinned cell. Ca2+-induced release of Ca2+ occurred under conditions that prevented any synthesis of ATP from ADP, was affected differentially by interventions that depressed the SR Ca2+ pump about equally, and required ionic conditions incompatible with all known Ca2+- releasing, uncoupled, partial reactions of the Ca2+ pump. Increasing the [free Ca2+]trigger up to an optimum increased the amount of Ca2+ released. A supraoptimum increase of [free Ca2+] trigger inactivated Ca2+-induced release of Ca2+, but partial inactivation was also observed at [free Ca2+] below that necessary for its activation. The amplitude of the Ca2+ release induced by a given increase of [free Ca2+] decreased when the rate of this increase was diminished. These results suggest that Ca2+-induced release of Ca2+ is through a channel across the SR membrane with time- and Ca2+-dependent activation and inactivation. The inactivating binding site would have a higher affinity for Ca2+ but a lower rate constant than the activating site. Inactivation appeared to be a first-order kinetic reaction of Ca2+ binding to a single site at the outer face of the SR with a Q10 of 1.68. The removal of inactivation was the slowest step of the cycle, responsible for a highly temperature-dependent (Q10 approximately 4.00) refractory period.

Full Text

The Full Text of this article is available as a PDF (2.4 MB).

Selected References

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

  1. BLINKS J. R., KOCH-WESER J. PHYSICAL FACTORS IN THE ANALYSIS OF THE ACTIONS OF DRUGS ON MYOCARDIAL CONTRACTILITY. Pharmacol Rev. 1963 Sep;15:531–599. [PubMed] [Google Scholar]
  2. Bayley P., Ahlström P., Martin S. R., Forsen S. The kinetics of calcium binding to calmodulin: Quin 2 and ANS stopped-flow fluorescence studies. Biochem Biophys Res Commun. 1984 Apr 16;120(1):185–191. doi: 10.1016/0006-291x(84)91431-1. [DOI] [PubMed] [Google Scholar]
  3. Blinks J. R., Rüdel R., Taylor S. R. Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin. J Physiol. 1978 Apr;277:291–323. doi: 10.1113/jphysiol.1978.sp012273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blinks J. R., Wier W. G., Hess P., Prendergast F. G. Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol. 1982;40(1-2):1–114. doi: 10.1016/0079-6107(82)90011-6. [DOI] [PubMed] [Google Scholar]
  5. Brandt P. W., Hibberd M. G. Proceedings: Effect of temperature on the pCa-tension relation of skinned ventricular muscle of the cat. J Physiol. 1976 Jun;258(2):76P–77P. [PubMed] [Google Scholar]
  6. Chiesi M., Wen Y. S. A phosphorylated conformational state of the (Ca2+-Mg2+)-ATPase of fast skeletal muscle sarcoplasmic reticulum can mediate rapid Ca2+ release. J Biol Chem. 1983 May 25;258(10):6078–6085. [PubMed] [Google Scholar]
  7. Edman K. A., Mattiazzi A., Nilsson E. The influence of temperature on the force-velocity relationship in rabbit papillary muscle. Acta Physiol Scand. 1974 Apr;90(4):750–756. doi: 10.1111/j.1748-1716.1974.tb05643.x. [DOI] [PubMed] [Google Scholar]
  8. Eisenberg B. R., Cohen I. S. The ultrastructure of the cardiac Purkinje strand in the dog: a morphometric analysis. Proc R Soc Lond B Biol Sci. 1983 Jan 22;217(1207):191–213. doi: 10.1098/rspb.1983.0006. [DOI] [PubMed] [Google Scholar]
  9. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  10. Eusebi F., Miledi R., Takahashi T. Aequorin-calcium transients in frog twitch muscle fibres. J Physiol. 1983 Jul;340:91–106. doi: 10.1113/jphysiol.1983.sp014751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fabiato A., Fabiato F. Excitation-contraction coupling of isolated cardiac fibers with disrupted or closed sarcolemmas. Calcium-dependent cyclic and tonic contractions. Circ Res. 1972 Sep;31(3):293–307. doi: 10.1161/01.res.31.3.293. [DOI] [PubMed] [Google Scholar]
  14. Fabiato A. Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol. 1981 Nov;78(5):457–497. doi: 10.1085/jgp.78.5.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Godt R. E., Lindley B. D. Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol. 1982 Aug;80(2):279–297. doi: 10.1085/jgp.80.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haiech J., Klee C. B., Demaille J. G. Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochemistry. 1981 Jun 23;20(13):3890–3897. doi: 10.1021/bi00516a035. [DOI] [PubMed] [Google Scholar]
  19. Harafuji H., Ogawa Y. Re-examination of the apparent binding constant of ethylene glycol bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid with calcium around neutral pH. J Biochem. 1980 May;87(5):1305–1312. doi: 10.1093/oxfordjournals.jbchem.a132868. [DOI] [PubMed] [Google Scholar]
  20. Hastings J. W., Mitchell G., Mattingly P. H., Blinks J. R., Van Leeuwen M. Response of aequorin bioluminescence to rapid changes in calcium concentration. Nature. 1969 Jun 14;222(5198):1047–1050. doi: 10.1038/2221047a0. [DOI] [PubMed] [Google Scholar]
  21. Johnson J. D., Charlton S. C., Potter J. D. A fluorescence stopped flow analysis of Ca2+ exchange with troponin C. J Biol Chem. 1979 May 10;254(9):3497–3502. [PubMed] [Google Scholar]
  22. Khan M. M., Martell A. E. Thermodynamic quantities associated with the interaction of adenosine triphosphate with metal ions. J Am Chem Soc. 1966 Feb 20;88(4):668–671. doi: 10.1021/ja00956a008. [DOI] [PubMed] [Google Scholar]
  23. Langer G. A., Brady A. J. The effects of temperature upon contraction and ionic exchange in rabbit ventricular myocardium. Relation to control of active state. J Gen Physiol. 1968 Oct;52(4):682–713. doi: 10.1085/jgp.52.4.682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lienhard G. E., Secemski I. I. P 1 ,P 5 -Di(adenosine-5')pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J Biol Chem. 1973 Feb 10;248(3):1121–1123. [PubMed] [Google Scholar]
  25. Makinose M. Possible functional states of the enzyme of the sarcoplasmic calcium pump. FEBS Lett. 1973 Dec 1;37(2):140–143. doi: 10.1016/0014-5793(73)80443-0. [DOI] [PubMed] [Google Scholar]
  26. Mattiazzi A. R., Nilsson E. The influence of temperature on the time course of the mechanical activity in rabbit papillary muscle. Acta Physiol Scand. 1976 Jul;97(3):310–318. doi: 10.1111/j.1748-1716.1976.tb10268.x. [DOI] [PubMed] [Google Scholar]
  27. Ogawa Y., Tanokura M. Calcium binding to calmodulin: effects of ionic strength, Mg2+, pH and temperature. J Biochem. 1984 Jan;95(1):19–28. doi: 10.1093/oxfordjournals.jbchem.a134584. [DOI] [PubMed] [Google Scholar]
  28. Rahn H., Reeves R. B., Howell B. J. Hydrogen ion regulation, temperature, and evolution. Am Rev Respir Dis. 1975 Aug;112(2):165–172. doi: 10.1164/arrd.1975.112.2.165. [DOI] [PubMed] [Google Scholar]
  29. Reeves R. B., Malan A. Model studies of intracellular acid-base temperature responses in ectotherms. Respir Physiol. 1976 Oct;28(1):49–63. doi: 10.1016/0034-5687(76)90084-0. [DOI] [PubMed] [Google Scholar]
  30. Reeves R. B. The interaction of body temperature and acid-base balance in ectothermic vertebrates. Annu Rev Physiol. 1977;39:559–586. doi: 10.1146/annurev.ph.39.030177.003015. [DOI] [PubMed] [Google Scholar]
  31. SHIMOMURA O., JOHNSON F. H., SAIGA Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol. 1962 Jun;59:223–239. doi: 10.1002/jcp.1030590302. [DOI] [PubMed] [Google Scholar]
  32. Saborowski F., Lang D., Albers C. Intracellular pH and buffer curves of cardiac muscle in rats as affected by temperature. Respir Physiol. 1973 Jul;18(2):161–170. doi: 10.1016/0034-5687(73)90046-7. [DOI] [PubMed] [Google Scholar]
  33. Stephenson D. G., Williams D. A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J Physiol. 1981 Aug;317:281–302. doi: 10.1113/jphysiol.1981.sp013825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. TRAUTWEIN W., DUDEL J. Aktionspotential und Mechanogramm des Katzenpapillarmuskels als Funktion der Temperatur. Pflugers Arch. 1954;260(2):104–115. [PubMed] [Google Scholar]
  35. Tsien R. Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry. 1980 May 27;19(11):2396–2404. doi: 10.1021/bi00552a018. [DOI] [PubMed] [Google Scholar]
  36. WOLD F., BALLOU C. E. Studies on the enzyme enolase. I. Equilibrium studies. J Biol Chem. 1957 Jul;227(1):301–312. [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES