Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1996 Oct;71(4):1714–1722. doi: 10.1016/S0006-3495(96)79373-6

Quantal release, incremental detection, and long-period Ca2+ oscillations in a model based on regulatory Ca2+-binding sites along the permeation pathway.

G Dupont 1, S Swillens 1
PMCID: PMC1233641  PMID: 8889149

Abstract

Quantal release, incremental detection, and oscillations are three types of Ca2+ responses that can be obtained in different conditions, after stimulation of the intracellular Ca2+ stores by submaximum concentrations of inositol 1,4,5-triphosphate (InsP3). All three phenomena are thought to occur through the regulatory properties of the InsP3 receptor/Ca2+ channel. In the present study, we perform further analysis of the model (Swillens et al., 1994, Proc. Natl. Acad. Sci. USA. 91:10074-10078) previously proposed for transient InsP3-induced Ca2+ release, based on the bell-shaped dependence of the InsP3 receptor activity on the Ca2+ level and on the existence of an intermediate Ca2+ domain located around the mouth of the channel. We show that Ca2+ oscillations also arise in the latter model. Conditions for the occurrence of the various behaviors are investigated. Numerical simulations also show that the existence of an intermediate Ca2+ domain can markedly increase the period of oscillations. Periods on the order of 1 min can indeed be accounted for by the model when one assigns realistic values to the kinetic constants of the InsP3 receptor, which, in the absence of a domain, lead to oscillations with periods of a few seconds. Finally, theoretical support in favor of a positive cooperativity in the regulation of the InsP3 receptor by Ca2+ is presented.

Full text

PDF
1718

Images in this article

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., Dupont G. Spatial and temporal signalling by calcium. Curr Opin Cell Biol. 1994 Apr;6(2):267–274. doi: 10.1016/0955-0674(94)90146-5. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Bootman M. D., Berridge M. J., Taylor C. W. All-or-nothing Ca2+ mobilization from the intracellular stores of single histamine-stimulated HeLa cells. J Physiol. 1992 May;450:163–178. doi: 10.1113/jphysiol.1992.sp019121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bootman M. D., Berridge M. J. The elemental principles of calcium signaling. Cell. 1995 Dec 1;83(5):675–678. doi: 10.1016/0092-8674(95)90179-5. [DOI] [PubMed] [Google Scholar]
  8. Bootman M. D., Cheek T. R., Moreton R. B., Bennett D. L., Berridge M. J. Smoothly graded Ca2+ release from inositol 1,4,5-trisphosphate-sensitive Ca2+ stores. J Biol Chem. 1994 Oct 7;269(40):24783–24791. [PubMed] [Google Scholar]
  9. Camello P., Gardner J., Petersen O. H., Tepikin A. V. Calcium dependence of calcium extrusion and calcium uptake in mouse pancreatic acinar cells. J Physiol. 1996 Feb 1;490(Pt 3):585–593. doi: 10.1113/jphysiol.1996.sp021169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carafoli E. Intracellular calcium homeostasis. Annu Rev Biochem. 1987;56:395–433. doi: 10.1146/annurev.bi.56.070187.002143. [DOI] [PubMed] [Google Scholar]
  11. Combettes L., Claret M., Champeil P. Calcium control on InsP3-induced discharge of calcium from permeabilised hepatocyte pools. Cell Calcium. 1993 Apr;14(4):279–292. doi: 10.1016/0143-4160(93)90049-c. [DOI] [PubMed] [Google Scholar]
  12. Combettes L., Claret M., Champeil P. Do submaximal InsP3 concentrations only induce the partial discharge of permeabilized hepatocyte calcium pools because of the concomitant reduction of intraluminal Ca2+ concentration? FEBS Lett. 1992 Apr 27;301(3):287–290. doi: 10.1016/0014-5793(92)80258-i. [DOI] [PubMed] [Google Scholar]
  13. Combettes L., Hannaert-Merah Z., Coquil J. F., Rousseau C., Claret M., Swillens S., Champeil P. Rapid filtration studies of the effect of cytosolic Ca2+ on inositol 1,4,5-trisphosphate-induced 45Ca2+ release from cerebellar microsomes. J Biol Chem. 1994 Jul 1;269(26):17561–17571. [PubMed] [Google Scholar]
  14. 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]
  15. Dupont G., Goldbeter A. Oscillations and waves of cytosolic calcium: insights from theoretical models. Bioessays. 1992 Jul;14(7):485–493. doi: 10.1002/bies.950140711. [DOI] [PubMed] [Google Scholar]
  16. Dupont G., Goldbeter A. Properties of intracellular Ca2+ waves generated by a model based on Ca(2+)-induced Ca2+ release. Biophys J. 1994 Dec;67(6):2191–2204. doi: 10.1016/S0006-3495(94)80705-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Endo M., Iino M. Properties of calcium release channels of the intracellular calcium store in muscle cells. Adv Second Messenger Phosphoprotein Res. 1990;24:122–127. [PubMed] [Google Scholar]
  18. Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol. 1975 Aug;249(3):469–495. doi: 10.1113/jphysiol.1975.sp011026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Favre C. J., Jerström P., Foti M., Stendhal O., Huggler E., Lew D. P., Krause K. H. Organization of Ca2+ stores in myeloid cells: association of SERCA2b and the type-1 inositol-1,4,5-trisphosphate receptor. Biochem J. 1996 May 15;316(Pt 1):137–142. doi: 10.1042/bj3160137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Goldbeter A., Dupont G. Allosteric regulation, cooperativity, and biochemical oscillations. Biophys Chem. 1990 Aug 31;37(1-3):341–353. doi: 10.1016/0301-4622(90)88033-o. [DOI] [PubMed] [Google Scholar]
  22. Goldbeter A., Dupont G., Berridge M. J. Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1461–1465. doi: 10.1073/pnas.87.4.1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Horne J. H., Meyer T. Luminal calcium regulates the inositol trisphosphate receptor of rat basophilic leukemia cells at a cytosolic site. Biochemistry. 1995 Oct 3;34(39):12738–12746. doi: 10.1021/bi00039a033. [DOI] [PubMed] [Google Scholar]
  24. Irvine R. F. 'Quantal' Ca2+ release and the control of Ca2+ entry by inositol phosphates--a possible mechanism. FEBS Lett. 1990 Apr 9;263(1):5–9. doi: 10.1016/0014-5793(90)80692-c. [DOI] [PubMed] [Google Scholar]
  25. Kindman L. A., Meyer T. Use of intracellular Ca2+ stores from rat basophilic leukemia cells to study the molecular mechanism leading to quantal Ca2+ release by inositol 1,4,5-trisphosphate. Biochemistry. 1993 Feb 9;32(5):1270–1277. doi: 10.1021/bi00056a011. [DOI] [PubMed] [Google Scholar]
  26. Kuba K., Takeshita S. Simulation of intracellular Ca2+ oscillation in a sympathetic neurone. J Theor Biol. 1981 Dec 21;93(4):1009–1031. doi: 10.1016/0022-5193(81)90352-0. [DOI] [PubMed] [Google Scholar]
  27. Lytton J., Westlin M., Burk S. E., Shull G. E., MacLennan D. H. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J Biol Chem. 1992 Jul 15;267(20):14483–14489. [PubMed] [Google Scholar]
  28. Meyer T., Stryer L. Calcium spiking. Annu Rev Biophys Biophys Chem. 1991;20:153–174. doi: 10.1146/annurev.bb.20.060191.001101. [DOI] [PubMed] [Google Scholar]
  29. Meyer T., Stryer L. Transient calcium release induced by successive increments of inositol 1,4,5-trisphosphate. Proc Natl Acad Sci U S A. 1990 May;87(10):3841–3845. doi: 10.1073/pnas.87.10.3841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Muallem S., Pandol S. J., Beeker T. G. Hormone-evoked calcium release from intracellular stores is a quantal process. J Biol Chem. 1989 Jan 5;264(1):205–212. [PubMed] [Google Scholar]
  31. Rossier M. F., Bird G. S., Putney J. W., Jr Subcellular distribution of the calcium-storing inositol 1,4,5-trisphosphate-sensitive organelle in rat liver. Possible linkage to the plasma membrane through the actin microfilaments. Biochem J. 1991 Mar 15;274(Pt 3):643–650. doi: 10.1042/bj2740643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schrenzel J., Demaurex N., Foti M., Van Delden C., Jacquet J., Mayr G., Lew D. P., Krause K. H. Highly cooperative Ca2+ elevations in response to Ins(1,4,5)P3 microperfusion through a patch-clamp pipette. Biophys J. 1995 Dec;69(6):2378–2391. doi: 10.1016/S0006-3495(95)80107-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith G. D., Wagner J., Keizer J. Validity of the rapid buffering approximation near a point source of calcium ions. Biophys J. 1996 Jun;70(6):2527–2539. doi: 10.1016/S0006-3495(96)79824-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sneyd J., Keizer J., Sanderson M. J. Mechanisms of calcium oscillations and waves: a quantitative analysis. FASEB J. 1995 Nov;9(14):1463–1472. doi: 10.1096/fasebj.9.14.7589988. [DOI] [PubMed] [Google Scholar]
  35. Steenbergen J. M., Fay F. S. The quantal nature of calcium release to caffeine in single smooth muscle cells results from activation of the sarcoplasmic reticulum Ca(2+)-ATPase. J Biol Chem. 1996 Jan 26;271(4):1821–1824. doi: 10.1074/jbc.271.4.1821. [DOI] [PubMed] [Google Scholar]
  36. Stucki J. W., Somogyi R. A dialogue on Ca2+ oscillations: an attempt to understand the essentials of mechanisms leading to hormone-induced intracellular Ca2+ oscillations in various kinds of cell on a theoretical level. Biochim Biophys Acta. 1994 Jan 4;1183(3):453–472. doi: 10.1016/0005-2728(94)90073-6. [DOI] [PubMed] [Google Scholar]
  37. Swillens S., Combettes L., Champeil P. Transient inositol 1,4,5-trisphosphate-induced Ca2+ release: a model based on regulatory Ca(2+)-binding sites along the permeation pathway. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10074–10078. doi: 10.1073/pnas.91.21.10074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Swillens S. Dynamic control of inositol 1,4,5-trisphosphate-induced Ca2+ release: a theoretical explanation for the quantal release of Ca2+. Mol Pharmacol. 1992 Jan;41(1):110–114. [PubMed] [Google Scholar]
  39. Swillens S., Mercan D. Computer simulation of a cytosolic calcium oscillator. Biochem J. 1990 Nov 1;271(3):835–838. doi: 10.1042/bj2710835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tang Y., Stephenson J. L., Othmer H. G. Simplification and analysis of models of calcium dynamics based on IP3-sensitive calcium channel kinetics. Biophys J. 1996 Jan;70(1):246–263. doi: 10.1016/S0006-3495(96)79567-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Taylor C. W., Potter B. V. The size of inositol 1,4,5-trisphosphate-sensitive Ca2+ stores depends on inositol 1,4,5-trisphosphate concentration. Biochem J. 1990 Feb 15;266(1):189–194. doi: 10.1042/bj2660189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tripathy A., Meissner G. Sarcoplasmic reticulum lumenal Ca2+ has access to cytosolic activation and inactivation sites of skeletal muscle Ca2+ release channel. Biophys J. 1996 Jun;70(6):2600–2615. doi: 10.1016/S0006-3495(96)79831-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tsien R. W., Tsien R. Y. Calcium channels, stores, and oscillations. Annu Rev Cell Biol. 1990;6:715–760. doi: 10.1146/annurev.cb.06.110190.003435. [DOI] [PubMed] [Google Scholar]

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

RESOURCES