Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1994 Aug 1;301(Pt 3):879–883. doi: 10.1042/bj3010879

Quantal Ca2+ mobilization by ryanodine receptors is due to all-or-none release from functionally discrete intracellular stores.

T R Cheek 1, M J Berridge 1, R B Moreton 1, K A Stauderman 1, M M Murawsky 1, M D Bootman 1
PMCID: PMC1137068  PMID: 8053911

Abstract

Low caffeine concentrations were unable to completely release the caffeine- and ryanodine-sensitive intracellular Ca2+ pool in intact adrenal chromaffin cells. This 'quantal' Ca2+ release is the same as that previously observed with inositol Ins(1,4,5)P3-induced Ca2+ release. The molecular mechanism underlying quantal Ca2+ release from the ryanodine receptor was investigated using fura-2 imaging of single chromaffin cells. Our data indicate that the intracellular caffeine-sensitive Ca2+ pool is composed of functionally discrete stores, that possess heterogeneous sensitivities to caffeine. These stores are mobilized by caffeine in a concentration-dependent fashion, and, when stimulated, individual stores release their Ca2+ in an 'all-or-none' manner. Such quantal Ca2+ release may be responsible for graded Ca2+ responses in single cells.

Full text

PDF
883

Selected References

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

  1. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Bootman M. Intracellular calcium. Questions about quantal Ca2+ release. Curr Biol. 1994 Feb 1;4(2):169–172. doi: 10.1016/s0960-9822(94)00041-2. [DOI] [PubMed] [Google Scholar]
  5. Buck E., Zimanyi I., Abramson J. J., Pessah I. N. Ryanodine stabilizes multiple conformational states of the skeletal muscle calcium release channel. J Biol Chem. 1992 Nov 25;267(33):23560–23567. [PubMed] [Google Scholar]
  6. Burgess G. M., Bird G. S., Obie J. F., Putney J. W., Jr The mechanism for synergism between phospholipase C- and adenylylcyclase-linked hormones in liver. Cyclic AMP-dependent kinase augments inositol trisphosphate-mediated Ca2+ mobilization without increasing the cellular levels of inositol polyphosphates. J Biol Chem. 1991 Mar 15;266(8):4772–4781. [PubMed] [Google Scholar]
  7. Cannell M. B., Berlin J. R., Lederer W. J. Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science. 1987 Dec 4;238(4832):1419–1423. doi: 10.1126/science.2446391. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cheek T. R., Moreton R. B., Berridge M. J., Stauderman K. A., Murawsky M. M., Bootman M. D. Quantal Ca2+ release from caffeine-sensitive stores in adrenal chromaffin cells. J Biol Chem. 1993 Dec 25;268(36):27076–27083. [PubMed] [Google Scholar]
  10. Cheek T. R., Morgan A., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Spatial localization of agonist-induced Ca2+ entry in bovine adrenal chromaffin cells. Different patterns induced by histamine and angiotensin II, and relationship to catecholamine release. J Cell Sci. 1993 Aug;105(Pt 4):913–921. doi: 10.1242/jcs.105.4.913. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Cleemann L., Morad M. Role of Ca2+ channel in cardiac excitation-contraction coupling in the rat: evidence from Ca2+ transients and contraction. J Physiol. 1991 Jan;432:283–312. doi: 10.1113/jphysiol.1991.sp018385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ferris C. D., Cameron A. M., Huganir R. L., Snyder S. H. Quantal calcium release by purified reconstituted inositol 1,4,5-trisphosphate receptors. Nature. 1992 Mar 26;356(6367):350–352. doi: 10.1038/356350a0. [DOI] [PubMed] [Google Scholar]
  14. Friel D. D., Tsien R. W. A caffeine- and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurones modulates effects of Ca2+ entry on [Ca2+]i. J Physiol. 1992 May;450:217–246. doi: 10.1113/jphysiol.1992.sp019125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  16. Györke S., Fill M. Response. Science. 1994 Feb 18;263(5149):987–988. doi: 10.1126/science.263.5149.987. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Henzi V., MacDermott A. B. Characteristics and function of Ca(2+)- and inositol 1,4,5-trisphosphate-releasable stores of Ca2+ in neurons. Neuroscience. 1992;46(2):251–273. doi: 10.1016/0306-4522(92)90049-8. [DOI] [PubMed] [Google Scholar]
  19. Hua S. Y., Nohmi M., Kuba K. Characteristics of Ca2+ release induced by Ca2+ influx in cultured bullfrog sympathetic neurones. J Physiol. 1993 May;464:245–272. doi: 10.1113/jphysiol.1993.sp019633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Lai F. A., Erickson H. P., Rousseau E., Liu Q. Y., Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature. 1988 Jan 28;331(6154):315–319. doi: 10.1038/331315a0. [DOI] [PubMed] [Google Scholar]
  22. Lamb G. D., Fryer M. W., Stephenson D. G. Ca(2+)-induced Ca2+ release in response to flash photolysis. Science. 1994 Feb 18;263(5149):986–988. doi: 10.1126/science.8310298. [DOI] [PubMed] [Google Scholar]
  23. Lipscombe D., Madison D. V., Poenie M., Reuter H., Tsien R. W., Tsien R. Y. Imaging of cytosolic Ca2+ transients arising from Ca2+ stores and Ca2+ channels in sympathetic neurons. Neuron. 1988 Jul;1(5):355–365. doi: 10.1016/0896-6273(88)90185-7. [DOI] [PubMed] [Google Scholar]
  24. Loomis-Husselbee J. W., Dawson A. P. A steady-state mechanism can account for the properties of inositol 2,4,5-trisphosphate-stimulated Ca2+ release from permeabilized L1210 cells. Biochem J. 1993 Feb 1;289(Pt 3):861–866. doi: 10.1042/bj2890861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Maeda N., Kawasaki T., Nakade S., Yokota N., Taguchi T., Kasai M., Mikoshiba K. Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum. J Biol Chem. 1991 Jan 15;266(2):1109–1116. [PubMed] [Google Scholar]
  26. McPherson P. S., Kim Y. K., Valdivia H., Knudson C. M., Takekura H., Franzini-Armstrong C., Coronado R., Campbell K. P. The brain ryanodine receptor: a caffeine-sensitive calcium release channel. Neuron. 1991 Jul;7(1):17–25. doi: 10.1016/0896-6273(91)90070-g. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Missiaen L., De Smedt H., Droogmans G., Casteels R. Ca2+ release induced by inositol 1,4,5-trisphosphate is a steady-state phenomenon controlled by luminal Ca2+ in permeabilized cells. Nature. 1992 Jun 18;357(6379):599–602. doi: 10.1038/357599a0. [DOI] [PubMed] [Google Scholar]
  29. Missiaen L., Taylor C. W., Berridge M. J. Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores. Nature. 1991 Jul 18;352(6332):241–244. doi: 10.1038/352241a0. [DOI] [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. Nelson T. E., Nelson K. E. Intra- and extraluminal sarcoplasmic reticulum membrane regulatory sites for Ca2(+)-induced Ca2+ release. FEBS Lett. 1990 Apr 24;263(2):292–294. doi: 10.1016/0014-5793(90)81396-6. [DOI] [PubMed] [Google Scholar]
  32. O'Sullivan A. J., Cheek T. R., Moreton R. B., Berridge M. J., Burgoyne R. D. Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2. EMBO J. 1989 Feb;8(2):401–411. doi: 10.1002/j.1460-2075.1989.tb03391.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Oldershaw K. A., Nunn D. L., Taylor C. W. Quantal Ca2+ mobilization stimulated by inositol 1,4,5-trisphosphate in permeabilized hepatocytes. Biochem J. 1991 Sep 15;278(Pt 3):705–708. doi: 10.1042/bj2780705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Oyamada H., Iino M., Endo M. Effects of ryanodine on the properties of Ca2+ release from the sarcoplasmic reticulum in skinned skeletal muscle fibres of the frog. J Physiol. 1993 Oct;470:335–348. doi: 10.1113/jphysiol.1993.sp019861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Parker I., Ivorra I. Confocal microfluorimetry of Ca2+ signals evoked in Xenopus oocytes by photoreleased inositol trisphosphate. J Physiol. 1993 Feb;461:133–165. doi: 10.1113/jphysiol.1993.sp019506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Parker I., Ivorra I. Localized all-or-none calcium liberation by inositol trisphosphate. Science. 1990 Nov 16;250(4983):977–979. doi: 10.1126/science.2237441. [DOI] [PubMed] [Google Scholar]
  37. Parker I., Yao Y. Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc Biol Sci. 1991 Dec 23;246(1317):269–274. doi: 10.1098/rspb.1991.0154. [DOI] [PubMed] [Google Scholar]
  38. Parys J. B., Missiaen L., De Smedt H., Casteels R. Loading dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in the clonal cell line A7r5. Implications for the mechanism of quantal Ca2+ release. J Biol Chem. 1993 Nov 25;268(33):25206–25212. [PubMed] [Google Scholar]
  39. Renard-Rooney D. C., Hajnóczky G., Seitz M. B., Schneider T. G., Thomas A. P. Imaging of inositol 1,4,5-trisphosphate-induced Ca2+ fluxes in single permeabilized hepatocytes. Demonstration of both quantal and nonquantal patterns of Ca2+ release. J Biol Chem. 1993 Nov 5;268(31):23601–23610. [PubMed] [Google Scholar]
  40. Short A. D., Klein M. G., Schneider M. F., Gill D. L. Inositol 1,4,5-trisphosphate-mediated quantal Ca2+ release measured by high resolution imaging of Ca2+ within organelles. J Biol Chem. 1993 Dec 5;268(34):25887–25893. [PubMed] [Google Scholar]
  41. 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]
  42. Stauderman K. A., Murawsky M. M. The inositol 1,4,5-trisphosphate-forming agonist histamine activates a ryanodine-sensitive Ca2+ release mechanism in bovine adrenal chromaffin cells. J Biol Chem. 1991 Oct 15;266(29):19150–19153. [PubMed] [Google Scholar]
  43. 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]
  44. Taylor C. W., Richardson A. Structure and function of inositol trisphosphate receptors. Pharmacol Ther. 1991;51(1):97–137. doi: 10.1016/0163-7258(91)90043-l. [DOI] [PubMed] [Google Scholar]
  45. Tregear R. T., Dawson A. P., Irvine R. F. Quantal release of Ca2+ from intracellular stores by InsP3: tests of the concept of control of Ca2+ release by intraluminal Ca2+. Proc Biol Sci. 1991 Mar 22;243(1308):263–268. doi: 10.1098/rspb.1991.0040. [DOI] [PubMed] [Google Scholar]
  46. Wang J., Best P. M. Inactivation of the sarcoplasmic reticulum calcium channel by protein kinase. Nature. 1992 Oct 22;359(6397):739–741. doi: 10.1038/359739a0. [DOI] [PubMed] [Google Scholar]
  47. Witcher D. R., Kovacs R. J., Schulman H., Cefali D. C., Jones L. R. Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem. 1991 Jun 15;266(17):11144–11152. [PubMed] [Google Scholar]

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

RESOURCES