Skip to main content
Molecular Biology of the Cell logoLink to Molecular Biology of the Cell
. 1995 Aug;6(8):945–951. doi: 10.1091/mbc.6.8.945

InsP3-induced Ca2+ excitability of the endoplasmic reticulum.

J Keizer 1, Y X Li 1, S Stojilković 1, J Rinzel 1
PMCID: PMC301254  PMID: 7579710

Abstract

Oscillations in intracellular Ca2+ can be induced by a variety of cellular signalling processes (Woods et al., 1986; Berridge 1988; Jacob et al., 1988) and appear to play a role in secretion (Stojilković et al., 1994), fertilization (Miyazaki et al., 1993), and smooth muscle contraction (Iino and Tsukioka, 1994). Recently, great progress has been made in understanding the mechanisms involved in a particular class of Ca2+ oscillation, associated with the second messenger inositol 1,4,5-trisphosphate (InsP3) (Berridge, 1993). Working in concert with intracellular Ca2+, InsP3 controls Ca2+ release via the InsP3 receptor in the endoplasmic reticulum (ER) (Berridge and Irvine, 1989). The IP3 receptor is regulated by its coagonists InsP3 and Ca2+, which both activate and inhibit Ca2+ release (Finch et al., 1991; Bezprozvanny et al., 1991; De Young and Keizer, 1992). These processes, together with the periodic activation of Ca2+ uptake into the ER, have been identified as key features in the mechanism of InsP3-induced Ca2+ oscillations in pituitary gonadotrophs (Li et al., 1994), Xenopus laevis oocytes (Lechleiter and Clapham, 1992; Atri et al., 1993), and other cell types (Keizer and De Young, 1993). Earlier discussions and models of InsP3-induced Ca2+ oscillations focused on the nature and number of internal releasable pools of Ca2+ (Goldbeter et al., 1990; Swillens and Mercan, 1990; Somogyi and Stucki, 1991), the importance of oscillations in InsP3 (Meyer and Stryer, 1988), and other issues not based on detailed experimental findings in specific cells types.

Full text

PDF
945

Selected References

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

  1. Allbritton N. L., Meyer T., Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science. 1992 Dec 11;258(5089):1812–1815. doi: 10.1126/science.1465619. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Berridge M. J., Cobbold P. H., Cuthbertson K. S. Spatial and temporal aspects of cell signalling. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 26;320(1199):325–343. doi: 10.1098/rstb.1988.0080. [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. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  6. Bertram R., Smolen P., Sherman A., Mears D., Atwater I., Martin F., Soria B. A role for calcium release-activated current (CRAC) in cholinergic modulation of electrical activity in pancreatic beta-cells. Biophys J. 1995 Jun;68(6):2323–2332. doi: 10.1016/S0006-3495(95)80414-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bezprozvanny I., Ehrlich B. E. Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium. J Gen Physiol. 1994 Nov;104(5):821–856. doi: 10.1085/jgp.104.5.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Bird G. J., Obie J. F., Putney J. W., Jr Functional homogeneity of the non-mitochondrial Ca2+ pool in intact mouse lacrimal acinar cells. J Biol Chem. 1992 Sep 15;267(26):18382–18386. [PubMed] [Google Scholar]
  10. Camacho P., Lechleiter J. D. Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science. 1993 Apr 9;260(5105):226–229. doi: 10.1126/science.8385800. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Chadwick C. C., Saito A., Fleischer S. Isolation and characterization of the inositol trisphosphate receptor from smooth muscle. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2132–2136. doi: 10.1073/pnas.87.6.2132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Cockcroft S., Thomas G. M. Inositol-lipid-specific phospholipase C isoenzymes and their differential regulation by receptors. Biochem J. 1992 Nov 15;288(Pt 1):1–14. doi: 10.1042/bj2880001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Danoff S. K., Ferris C. D., Donath C., Fischer G. A., Munemitsu S., Ullrich A., Snyder S. H., Ross C. A. Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuronal forms derived by alternative splicing differ in phosphorylation. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2951–2955. doi: 10.1073/pnas.88.7.2951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Dolmetsch R. E., Lewis R. S. Signaling between intracellular Ca2+ stores and depletion-activated Ca2+ channels generates [Ca2+]i oscillations in T lymphocytes. J Gen Physiol. 1994 Mar;103(3):365–388. doi: 10.1085/jgp.103.3.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Gilchrist J. S., Czubryt M. P., Pierce G. N. Calcium and calcium-binding proteins in the nucleus. Mol Cell Biochem. 1994 Jun 15;135(1):79–88. doi: 10.1007/BF00925963. [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. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hajnóczky G., Thomas A. P. The inositol trisphosphate calcium channel is inactivated by inositol trisphosphate. Nature. 1994 Aug 11;370(6489):474–477. doi: 10.1038/370474a0. [DOI] [PubMed] [Google Scholar]
  25. Hanson P. I., Meyer T., Stryer L., Schulman H. Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron. 1994 May;12(5):943–956. doi: 10.1016/0896-6273(94)90306-9. [DOI] [PubMed] [Google Scholar]
  26. Hofer A. M., Machen T. E. Technique for in situ measurement of calcium in intracellular inositol 1,4,5-trisphosphate-sensitive stores using the fluorescent indicator mag-fura-2. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2598–2602. doi: 10.1073/pnas.90.7.2598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Iida T., Stojilković S. S., Izumi S., Catt K. J. Spontaneous and agonist-induced calcium oscillations in pituitary gonadotrophs. Mol Endocrinol. 1991 Jul;5(7):949–958. doi: 10.1210/mend-5-7-949. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Jacob R., Merritt J. E., Hallam T. J., Rink T. J. Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells. Nature. 1988 Sep 1;335(6185):40–45. doi: 10.1038/335040a0. [DOI] [PubMed] [Google Scholar]
  31. Keizer J., De Young G. W. Two roles of Ca2+ in agonist stimulated Ca2+ oscillations. Biophys J. 1992 Mar;61(3):649–660. doi: 10.1016/S0006-3495(92)81870-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Keizer J., De Young G. Effect of voltage-gated plasma membrane Ca2+ fluxes on IP3-linked Ca2+ oscillations. Cell Calcium. 1993 May;14(5):397–410. doi: 10.1016/0143-4160(93)90044-7. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Kukuljan M., Rojas E., Catt K. J., Stojilkovic S. S. Membrane potential regulates inositol 1,4,5-trisphosphate-controlled cytoplasmic Ca2+ oscillations in pituitary gonadotrophs. J Biol Chem. 1994 Feb 18;269(7):4860–4865. [PubMed] [Google Scholar]
  35. 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]
  36. Li Y. X., Rinzel J. Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J Theor Biol. 1994 Feb 21;166(4):461–473. doi: 10.1006/jtbi.1994.1041. [DOI] [PubMed] [Google Scholar]
  37. Li Y. X., Rinzel J., Keizer J., Stojilković S. S. Calcium oscillations in pituitary gonadotrophs: comparison of experiment and theory. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):58–62. doi: 10.1073/pnas.91.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Marshall I. C., Taylor C. W. Regulation of inositol 1,4,5-trisphosphate receptors. J Exp Biol. 1993 Nov;184:161–182. doi: 10.1242/jeb.184.1.161. [DOI] [PubMed] [Google Scholar]
  40. Marshall I. C., Taylor C. W. Two calcium-binding sites mediate the interconversion of liver inositol 1,4,5-trisphosphate receptors between three conformational states. Biochem J. 1994 Jul 15;301(Pt 2):591–598. doi: 10.1042/bj3010591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Meyer T. Cell signaling by second messenger waves. Cell. 1991 Feb 22;64(4):675–678. doi: 10.1016/0092-8674(91)90496-l. [DOI] [PubMed] [Google Scholar]
  42. Meyer T., Stryer L. Molecular model for receptor-stimulated calcium spiking. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5051–5055. doi: 10.1073/pnas.85.14.5051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mignery G. A., Südhof T. C., Takei K., De Camilli P. Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature. 1989 Nov 9;342(6246):192–195. doi: 10.1038/342192a0. [DOI] [PubMed] [Google Scholar]
  44. Missiaen L., De Smedt H., Droogmans G., Casteels R. Luminal Ca2+ controls the activation of the inositol 1,4,5-trisphosphate receptor by cytosolic Ca2+. J Biol Chem. 1992 Nov 15;267(32):22961–22966. [PubMed] [Google Scholar]
  45. Miyazaki S., Shirakawa H., Nakada K., Honda Y. Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian eggs. Dev Biol. 1993 Jul;158(1):62–78. doi: 10.1006/dbio.1993.1168. [DOI] [PubMed] [Google Scholar]
  46. Neher E., Augustine G. J. Calcium gradients and buffers in bovine chromaffin cells. J Physiol. 1992 May;450:273–301. doi: 10.1113/jphysiol.1992.sp019127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Parker I., Ivorra I. Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: a possible mechanism for oscillatory release of Ca2+. Proc Natl Acad Sci U S A. 1990 Jan;87(1):260–264. doi: 10.1073/pnas.87.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Payne R., Walz B., Levy S., Fein A. The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 26;320(1199):359–379. doi: 10.1098/rstb.1988.0082. [DOI] [PubMed] [Google Scholar]
  49. Putney J. W., Jr, Bird G. S. The inositol phosphate-calcium signaling system in nonexcitable cells. Endocr Rev. 1993 Oct;14(5):610–631. doi: 10.1210/edrv-14-5-610. [DOI] [PubMed] [Google Scholar]
  50. Sneyd J., Girard S., Clapham D. Calcium wave propagation by calcium-induced calcium release: an unusual excitable system. Bull Math Biol. 1993 Mar;55(2):315–344. doi: 10.1007/BF02460886. [DOI] [PubMed] [Google Scholar]
  51. Somogyi R., Stucki J. W. Hormone-induced calcium oscillations in liver cells can be explained by a simple one pool model. J Biol Chem. 1991 Jun 15;266(17):11068–11077. [PubMed] [Google Scholar]
  52. Stojilkovic S. S., Reinhart J., Catt K. J. Gonadotropin-releasing hormone receptors: structure and signal transduction pathways. Endocr Rev. 1994 Aug;15(4):462–499. doi: 10.1210/edrv-15-4-462. [DOI] [PubMed] [Google Scholar]
  53. Stojilkovic S. S., Tomic M., Kukuljan M., Catt K. J. Control of calcium spiking frequency in pituitary gonadotrophs by a single-pool cytoplasmic oscillator. Mol Pharmacol. 1994 May;45(5):1013–1021. [PubMed] [Google Scholar]
  54. Stojilković S. S., Kukuljan M., Iida T., Rojas E., Catt K. J. Integration of cytoplasmic calcium and membrane potential oscillations maintains calcium signaling in pituitary gonadotrophs. Proc Natl Acad Sci U S A. 1992 May 1;89(9):4081–4085. doi: 10.1073/pnas.89.9.4081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Stojilković S. S., Kukuljan M., Tomić M., Rojas E., Catt K. J. Mechanism of agonist-induced [Ca2+]i oscillations in pituitary gonadotrophs. J Biol Chem. 1993 Apr 15;268(11):7713–7720. [PubMed] [Google Scholar]
  56. 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]
  57. 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]
  58. Terasaki M., Slater N. T., Fein A., Schmidek A., Reese T. S. Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7510–7514. doi: 10.1073/pnas.91.16.7510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Tse A., Hille B. Role of voltage-gated Na+ and Ca2+ channels in gonadotropin-releasing hormone-induced membrane potential changes in identified rat gonadotropes. Endocrinology. 1993 Apr;132(4):1475–1481. doi: 10.1210/endo.132.4.8384989. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. 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]
  62. 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]
  63. Tsunoda Y. Oscillatory Ca2+ signaling and its cellular function. New Biol. 1991 Jan;3(1):3–17. [PubMed] [Google Scholar]
  64. Wagenknecht T., Grassucci R., Frank J., Saito A., Inui M., Fleischer S. Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature. 1989 Mar 9;338(6211):167–170. doi: 10.1038/338167a0. [DOI] [PubMed] [Google Scholar]
  65. Wagner J., Keizer J. Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys J. 1994 Jul;67(1):447–456. doi: 10.1016/S0006-3495(94)80500-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Watras J., Bezprozvanny I., Ehrlich B. E. Inositol 1,4,5-trisphosphate-gated channels in cerebellum: presence of multiple conductance states. J Neurosci. 1991 Oct;11(10):3239–3245. doi: 10.1523/JNEUROSCI.11-10-03239.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Woods N. M., Cuthbertson K. S., Cobbold P. H. Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature. 1986 Feb 13;319(6054):600–602. doi: 10.1038/319600a0. [DOI] [PubMed] [Google Scholar]
  68. Yao Y., Choi J., Parker I. Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J Physiol. 1995 Feb 1;482(Pt 3):533–553. doi: 10.1113/jphysiol.1995.sp020538. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular Biology of the Cell are provided here courtesy of American Society for Cell Biology

RESOURCES