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. 1995 Jan;68(1):40–45. doi: 10.1016/S0006-3495(95)80196-7

Temperature dependence of Ca2+ wave properties in cardiomyocytes: implications for the mechanism of autocatalytic Ca2+ release in wave propagation.

J Engel 1, A J Sowerby 1, S A Finch 1, M Fechner 1, A Stier 1
PMCID: PMC1281658  PMID: 7711265

Abstract

Digital imaging microscopy of fluo-3 fluorescence was used to study the velocity and shape of intracellular Ca2+ waves in isolated rat cardiomyocytes as a function of temperature. Decreasing the temperature from 37 to 17 degrees C reduced the longitudinal wave velocity by a factor of 1.8 and remarkably slowed the decay of [Ca2+]i in the trailing flank of a wave. Using image analysis, rise times, and half-maximum decay times of local Ca2+ transients, which characterize the processes of local Ca2+ release and removal, were determined as a function of temperature. Apparent activation energies for wave front propagation, local Ca2+ release, and local Ca2+ removal were derived from Arrhenius plots and amounted to -23, -28, and -46 kJ/mol, respectively. The high activation energy of Ca2+ removal, which arises from the activity of the sarcoplasmic reticulum (SR) Ca2+ ATPase, relative to those of longitudinal wave propagation and local Ca2+ release excludes the hypothetical mechanism of regenerative "spontaneous Ca2+ release," in which Ca2+ that has been taken up from the approaching wavefront triggers Ca2+ release at a luminal site of the SR. It is consistent, however, with the hypothesis that Ca2+ wave propagation is based on Ca(2+)-induced Ca2+ release where Ca2+ triggers release on the cytosolic face of the SR.

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Selected References

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  1. Bers D. M., Bridge J. H. Relaxation of rabbit ventricular muscle by Na-Ca exchange and sarcoplasmic reticulum calcium pump. Ryanodine and voltage sensitivity. Circ Res. 1989 Aug;65(2):334–342. doi: 10.1161/01.res.65.2.334. [DOI] [PubMed] [Google Scholar]
  2. Engel J., Fechner M., Sowerby A. J., Finch S. A., Stier A. Anisotropic propagation of Ca2+ waves in isolated cardiomyocytes. Biophys J. 1994 Jun;66(6):1756–1762. doi: 10.1016/S0006-3495(94)80997-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Fabiato A. Two kinds of calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cardiac cells. Adv Exp Med Biol. 1992;311:245–262. doi: 10.1007/978-1-4615-3362-7_18. [DOI] [PubMed] [Google Scholar]
  6. Grouselle M., Stuyvers B., Bonoron-Adele S., Besse P., Georgescauld D. Digital-imaging microscopy analysis of calcium release from sarcoplasmic reticulum in single rat cardiac myocytes. Pflugers Arch. 1991 Mar;418(1-2):109–119. doi: 10.1007/BF00370459. [DOI] [PubMed] [Google Scholar]
  7. Ishide N., Miura M., Sakurai M., Takishima T. Initiation and development of calcium waves in rat myocytes. Am J Physiol. 1992 Aug;263(2 Pt 2):H327–H332. doi: 10.1152/ajpheart.1992.263.2.H327. [DOI] [PubMed] [Google Scholar]
  8. Ishide N., Urayama T., Inoue K., Komaru T., Takishima T. Propagation and collision characteristics of calcium waves in rat myocytes. Am J Physiol. 1990 Sep;259(3 Pt 2):H940–H950. doi: 10.1152/ajpheart.1990.259.3.H940. [DOI] [PubMed] [Google Scholar]
  9. Jaffe L. F. Classes and mechanisms of calcium waves. Cell Calcium. 1993 Nov;14(10):736–745. doi: 10.1016/0143-4160(93)90099-r. [DOI] [PubMed] [Google Scholar]
  10. Lakatta E. G. Functional implications of spontaneous sarcoplasmic reticulum Ca2+ release in the heart. Cardiovasc Res. 1992 Mar;26(3):193–214. doi: 10.1093/cvr/26.3.193. [DOI] [PubMed] [Google Scholar]
  11. Lechleiter J. D., Clapham D. E. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes. Cell. 1992 Apr 17;69(2):283–294. doi: 10.1016/0092-8674(92)90409-6. [DOI] [PubMed] [Google Scholar]
  12. Lipp P., Niggli E. Microscopic spiral waves reveal positive feedback in subcellular calcium signaling. Biophys J. 1993 Dec;65(6):2272–2276. doi: 10.1016/S0006-3495(93)81316-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Minta A., Kao J. P., Tsien R. Y. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J Biol Chem. 1989 May 15;264(14):8171–8178. [PubMed] [Google Scholar]
  14. Powell T., Noble D. Calcium movements during each heart beat. Mol Cell Biochem. 1989 Sep 7;89(2):103–108. doi: 10.1007/BF00220760. [DOI] [PubMed] [Google Scholar]
  15. Sipido K. R., Wier W. G. Flux of Ca2+ across the sarcoplasmic reticulum of guinea-pig cardiac cells during excitation-contraction coupling. J Physiol. 1991 Apr;435:605–630. doi: 10.1113/jphysiol.1991.sp018528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Squier T. C., Bigelow D. J., Thomas D. D. Lipid fluidity directly modulates the overall protein rotational mobility of the Ca-ATPase in sarcoplasmic reticulum. J Biol Chem. 1988 Jul 5;263(19):9178–9186. [PubMed] [Google Scholar]
  17. Stern M. D., Capogrossi M. C., Lakatta E. G. Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells: mechanisms and consequences. Cell Calcium. 1988 Dec;9(5-6):247–256. doi: 10.1016/0143-4160(88)90005-x. [DOI] [PubMed] [Google Scholar]
  18. Stern M. D. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992 Aug;63(2):497–517. doi: 10.1016/S0006-3495(92)81615-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Takamatsu T., Wier W. G. Calcium waves in mammalian heart: quantification of origin, magnitude, waveform, and velocity. FASEB J. 1990 Mar;4(5):1519–1525. doi: 10.1096/fasebj.4.5.2307330. [DOI] [PubMed] [Google Scholar]
  20. Trafford A. W., O'Neill S. C., Eisner D. A. Factors affecting the propagation of locally activated systolic Ca transients in rat ventricular myocytes. Pflugers Arch. 1993 Oct;425(1-2):181–183. doi: 10.1007/BF00374521. [DOI] [PubMed] [Google Scholar]
  21. Wier W. G., Blatter L. A. Ca(2+)-oscillations and Ca(2+)-waves in mammalian cardiac and vascular smooth muscle cells. Cell Calcium. 1991 Feb-Mar;12(2-3):241–254. doi: 10.1016/0143-4160(91)90024-9. [DOI] [PubMed] [Google Scholar]
  22. Williams D. A., Delbridge L. M., Cody S. H., Harris P. J., Morgan T. O. Spontaneous and propagated calcium release in isolated cardiac myocytes viewed by confocal microscopy. Am J Physiol. 1992 Mar;262(3 Pt 1):C731–C742. doi: 10.1152/ajpcell.1992.262.3.C731. [DOI] [PubMed] [Google Scholar]
  23. Williams D. A. Mechanisms of calcium release and propagation in cardiac cells. Do studies with confocal microscopy add to our understanding? Cell Calcium. 1993 Nov;14(10):724–735. doi: 10.1016/0143-4160(93)90098-q. [DOI] [PubMed] [Google Scholar]

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