Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1996 Dec;71(6):3477–3487. doi: 10.1016/S0006-3495(96)79543-7

Ryanodine receptor adaptation and Ca2+(-)induced Ca2+ release-dependent Ca2+ oscillations.

J Keizer 1, L Levine 1
PMCID: PMC1233835  PMID: 8968617

Abstract

A simplified mechanism that mimics "adaptation" of the ryanodine receptor (RyR) has been developed and its significance for Ca2+(-)induced Ca2+ release and Ca2+ oscillations investigated. For parameters that reproduce experimental data for the RyR from cardiac cells, adaptation of the RyR in combination with sarco/endoplasmic reticulum Ca2+ ATPase Ca2+ pumps in the internal stores can give rise to either low [Cai2+] steady states or Ca2+ oscillations coexisting with unphysiologically high [Cai2+] steady states. In this closed-cell-type model rapid, adaptation-dependent Ca2+ oscillations occur only in limited ranges of parameters. In the presence of Ca2+ influx and efflux from outside the cell (open-cell model) Ca2+ oscillations occur for a wide range of physiological parameter values and have a period that is determined by the rate of Ca2+ refilling of the stores. Although the rate of adaptation of the RyR has a role in determining the shape and the period of the Ca2+ spike, it is not essential for their existence. This is in marked contrast with what is observed for the inositol 1,4,5-trisphosphate receptor for which the biphasic activation and inhibition of its activity by Ca2+ are sufficient to produce oscillations. Results for this model are compared with those based on Ca2+(-)induced Ca2+ release alone in the bullfrog sympathetic neuron. This kinetic model should be suitable for analyzing phenomena associated with "Ca2+ sparks," including their merger into Ca2+ waves in cardiac myocytes.

Full text

PDF
3477

Selected References

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

  1. Atri A., Amundson J., Clapham D., Sneyd J. A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys J. 1993 Oct;65(4):1727–1739. doi: 10.1016/S0006-3495(93)81191-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berridge M. J., Galione A. Cytosolic calcium oscillators. FASEB J. 1988 Dec;2(15):3074–3082. doi: 10.1096/fasebj.2.15.2847949. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  4. Bezprozvanny I., Watras J., Ehrlich B. E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature. 1991 Jun 27;351(6329):751–754. doi: 10.1038/351751a0. [DOI] [PubMed] [Google Scholar]
  5. Carafoli E. Biogenesis: plasma membrane calcium ATPase: 15 years of work on the purified enzyme. FASEB J. 1994 Oct;8(13):993–1002. [PubMed] [Google Scholar]
  6. Cheng H., Fill M., Valdivia H., Lederer W. J. Models of Ca2+ release channel adaptation. Science. 1995 Mar 31;267(5206):2009–2010. doi: 10.1126/science.7701326. [DOI] [PubMed] [Google Scholar]
  7. Cheng H., Lederer M. R., Lederer W. J., Cannell M. B. Calcium sparks and [Ca2+]i waves in cardiac myocytes. Am J Physiol. 1996 Jan;270(1 Pt 1):C148–C159. doi: 10.1152/ajpcell.1996.270.1.C148. [DOI] [PubMed] [Google Scholar]
  8. Cheng H., Lederer W. J., Cannell M. B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993 Oct 29;262(5134):740–744. doi: 10.1126/science.8235594. [DOI] [PubMed] [Google Scholar]
  9. Chu A., Fill M., Stefani E., Entman M. L. Cytoplasmic Ca2+ does not inhibit the cardiac muscle sarcoplasmic reticulum ryanodine receptor Ca2+ channel, although Ca(2+)-induced Ca2+ inactivation of Ca2+ release is observed in native vesicles. J Membr Biol. 1993 Jul;135(1):49–59. doi: 10.1007/BF00234651. [DOI] [PubMed] [Google Scholar]
  10. De Young G. W., Keizer J. A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9895–9899. doi: 10.1073/pnas.89.20.9895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Finch E. A., Turner T. J., Goldin S. M. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science. 1991 Apr 19;252(5004):443–446. doi: 10.1126/science.2017683. [DOI] [PubMed] [Google Scholar]
  12. Friel D. D., Tsien R. W. Phase-dependent contributions from Ca2+ entry and Ca2+ release to caffeine-induced [Ca2+]i oscillations in bullfrog sympathetic neurons. Neuron. 1992 Jun;8(6):1109–1125. doi: 10.1016/0896-6273(92)90132-w. [DOI] [PubMed] [Google Scholar]
  13. Friel D. D. [Ca2+]i oscillations in sympathetic neurons: an experimental test of a theoretical model. Biophys J. 1995 May;68(5):1752–1766. doi: 10.1016/S0006-3495(95)80352-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Györke S., Fill M. Response. Science. 1994 Feb 18;263(5149):987–988. doi: 10.1126/science.263.5149.987. [DOI] [PubMed] [Google Scholar]
  15. Györke S., Fill M. Ryanodine receptor adaptation: control mechanism of Ca(2+)-induced Ca2+ release in heart. Science. 1993 May 7;260(5109):807–809. doi: 10.1126/science.8387229. [DOI] [PubMed] [Google Scholar]
  16. Györke S., Vélez P., Suárez-Isla B., Fill M. Activation of single cardiac and skeletal ryanodine receptor channels by flash photolysis of caged Ca2+. Biophys J. 1994 Jun;66(6):1879–1886. doi: 10.1016/S0006-3495(94)80981-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hofer A. M., Machen T. E. Direct measurement of free Ca in organelles of gastric epithelial cells. Am J Physiol. 1994 Sep;267(3 Pt 1):G442–G451. doi: 10.1152/ajpgi.1994.267.3.G442. [DOI] [PubMed] [Google Scholar]
  18. Iino M. Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol. 1990 Jun;95(6):1103–1122. doi: 10.1085/jgp.95.6.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Iino M., Tsukioka M. Feedback control of inositol trisphosphate signalling bycalcium. Mol Cell Endocrinol. 1994 Jan;98(2):141–146. doi: 10.1016/0303-7207(94)90132-5. [DOI] [PubMed] [Google Scholar]
  20. Jafri M. S., Keizer J. Diffusion of inositol 1,4,5-trisphosphate but not Ca2+ is necessary for a class of inositol 1,4,5-trisphosphate-induced Ca2+ waves. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9485–9489. doi: 10.1073/pnas.91.20.9485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jafri M. S., Keizer J. On the roles of Ca2+ diffusion, Ca2+ buffers, and the endoplasmic reticulum in IP3-induced Ca2+ waves. Biophys J. 1995 Nov;69(5):2139–2153. doi: 10.1016/S0006-3495(95)80088-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Keizer J., Li Y. X., Stojilković S., Rinzel J. InsP3-induced Ca2+ excitability of the endoplasmic reticulum. Mol Biol Cell. 1995 Aug;6(8):945–951. doi: 10.1091/mbc.6.8.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Laver D. R., Roden L. D., Ahern G. P., Eager K. R., Junankar P. R., Dulhunty A. F. Cytoplasmic Ca2+ inhibits the ryanodine receptor from cardiac muscle. J Membr Biol. 1995 Sep;147(1):7–22. doi: 10.1007/BF00235394. [DOI] [PubMed] [Google Scholar]
  24. Li Y. X., Keizer J., Stojilković S. S., Rinzel J. Ca2+ excitability of the ER membrane: an explanation for IP3-induced Ca2+ oscillations. Am J Physiol. 1995 Nov;269(5 Pt 1):C1079–C1092. doi: 10.1152/ajpcell.1995.269.5.C1079. [DOI] [PubMed] [Google Scholar]
  25. Louis C. F. Caged calcium and the ryanodine receptor. Biophys J. 1994 Jun;66(6):1739–1740. doi: 10.1016/S0006-3495(94)80968-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogawa Y. Role of ryanodine receptors. Crit Rev Biochem Mol Biol. 1994;29(4):229–274. doi: 10.3109/10409239409083482. [DOI] [PubMed] [Google Scholar]
  27. Sachs F., Qin F., Palade P. Models of Ca2+ release channel adaptation. Science. 1995 Mar 31;267(5206):2010–2011. doi: 10.1126/science.7701327. [DOI] [PubMed] [Google Scholar]
  28. Scharff O., Foder B. Regulation of cytosolic calcium in blood cells. Physiol Rev. 1993 Jul;73(3):547–582. doi: 10.1152/physrev.1993.73.3.547. [DOI] [PubMed] [Google Scholar]
  29. Tang Y., Othmer H. G. A model of calcium dynamics in cardiac myocytes based on the kinetics of ryanodine-sensitive calcium channels. Biophys J. 1994 Dec;67(6):2223–2235. doi: 10.1016/S0006-3495(94)80707-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tse A., Tse F. W., Hille B. Calcium homeostasis in identified rat gonadotrophs. J Physiol. 1994 Jun 15;477(Pt 3):511–525. doi: 10.1113/jphysiol.1994.sp020212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tse F. W., Tse A., Hille B. Cyclic Ca2+ changes in intracellular stores of gonadotropes during gonadotropin-releasing hormone-stimulated Ca2+ oscillations. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9750–9754. doi: 10.1073/pnas.91.21.9750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Valdivia H. H., Kaplan J. H., Ellis-Davies G. C., Lederer W. J. Rapid adaptation of cardiac ryanodine receptors: modulation by Mg2+ and phosphorylation. Science. 1995 Mar 31;267(5206):1997–2000. doi: 10.1126/science.7701323. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES