Abstract
We have investigated the role of the ryanodine-sensitive intracellular Ca2+ release channel (ryanodine receptor) in the cytosolic Ca2+ oscillations evoked in pancreatic acinar cells by acetylcholine (ACh) or cholecystokinin (CCK). Ryanodine abolished or markedly inhibited the agonist evoked Ca2+ spiking, but enhanced the frequency of spikes evoked by direct internal inositol trisphosphate (InsP3) application. We have also investigated the possibility that cyclic ADP-ribose (cADP-ribose), the putative second messenger controlling the ryanodine receptor, plays a role in Ca2+ oscillations. We found that cADP-ribose could itself induce repetitive Ca2+ spikes localized in the secretory pole and that these spikes were blocked by ryanodine, but also by the InsP3 receptor antagonist heparin. Our results indicate that both the ryanodine and the InsP3 receptors are involved in Ca2+ spike generation.
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Selected References
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- Berridge M. J. Cell signalling. A tale of two messengers. Nature. 1993 Sep 30;365(6445):388–389. doi: 10.1038/365388a0. [DOI] [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Christophe J. P., Frandsen E. K., Conlon T. P., Krishna G., Gardner J. D. Action of cholecystokinin, cholinergic agents, and A-23187 on accumulation of guanosine 3':5'-monophosphate in dispersed guinea pig pancreatic acinar cells. J Biol Chem. 1976 Aug 10;251(15):4640–4645. [PubMed] [Google Scholar]
- Clapper D. L., Walseth T. F., Dargie P. J., Lee H. C. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem. 1987 Jul 15;262(20):9561–9568. [PubMed] [Google Scholar]
- D'Andrea P., Zacchetti D., Meldolesi J., Grohovaz F. Mechanism of [Ca2+]i oscillations in rat chromaffin cells. Complex Ca(2+)-dependent regulation of a ryanodine-insensitive oscillator. J Biol Chem. 1993 Jul 15;268(20):15213–15220. [PubMed] [Google Scholar]
- 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]
- Galione A. Cyclic ADP-ribose: a new way to control calcium. Science. 1993 Jan 15;259(5093):325–326. doi: 10.1126/science.8380506. [DOI] [PubMed] [Google Scholar]
- Galione A., McDougall A., Busa W. B., Willmott N., Gillot I., Whitaker M. Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science. 1993 Jul 16;261(5119):348–352. doi: 10.1126/science.8392748. [DOI] [PubMed] [Google Scholar]
- Galione A., White A., Willmott N., Turner M., Potter B. V., Watson S. P. cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature. 1993 Sep 30;365(6445):456–459. doi: 10.1038/365456a0. [DOI] [PubMed] [Google Scholar]
- Giannini G., Clementi E., Ceci R., Marziali G., Sorrentino V. Expression of a ryanodine receptor-Ca2+ channel that is regulated by TGF-beta. Science. 1992 Jul 3;257(5066):91–94. doi: 10.1126/science.1320290. [DOI] [PubMed] [Google Scholar]
- Kasai H., Li Y. X., Miyashita Y. Subcellular distribution of Ca2+ release channels underlying Ca2+ waves and oscillations in exocrine pancreas. Cell. 1993 Aug 27;74(4):669–677. doi: 10.1016/0092-8674(93)90514-q. [DOI] [PubMed] [Google Scholar]
- Kramer R. H., Mokkapatti R., Levitan E. S. Effects of caffeine on intracellular calcium, calcium current and calcium-dependent potassium current in anterior pituitary GH3 cells. Pflugers Arch. 1994 Jan;426(1-2):12–20. doi: 10.1007/BF00374665. [DOI] [PubMed] [Google Scholar]
- 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]
- Malgaroli A., Fesce R., Meldolesi J. Spontaneous [Ca2+]i fluctuations in rat chromaffin cells do not require inositol 1,4,5-trisphosphate elevations but are generated by a caffeine- and ryanodine-sensitive intracellular Ca2+ store. J Biol Chem. 1990 Feb 25;265(6):3005–3008. [PubMed] [Google Scholar]
- Marty A., Tan Y. P. The initiation of calcium release following muscarinic stimulation in rat lacrimal glands. J Physiol. 1989 Dec;419:665–687. doi: 10.1113/jphysiol.1989.sp017892. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matozaki T., Göke B., Tsunoda Y., Rodriguez M., Martinez J., Williams J. A. Two functionally distinct cholecystokinin receptors show different modes of action on Ca2+ mobilization and phospholipid hydrolysis in isolated rat pancreatic acini. Studies using a new cholecystokinin analog, JMV-180. J Biol Chem. 1990 Apr 15;265(11):6247–6254. [PubMed] [Google Scholar]
- Mészáros L. G., Bak J., Chu A. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature. 1993 Jul 1;364(6432):76–79. doi: 10.1038/364076a0. [DOI] [PubMed] [Google Scholar]
- Nathanson M. H., Padfield P. J., O'Sullivan A. J., Burgstahler A. D., Jamieson J. D. Mechanism of Ca2+ wave propagation in pancreatic acinar cells. J Biol Chem. 1992 Sep 5;267(25):18118–18121. [PubMed] [Google Scholar]
- Osipchuk Y. V., Wakui M., Yule D. I., Gallacher D. V., Petersen O. H. Cytoplasmic Ca2+ oscillations evoked by receptor stimulation, G-protein activation, internal application of inositol trisphosphate or Ca2+: simultaneous microfluorimetry and Ca2+ dependent Cl- current recording in single pancreatic acinar cells. EMBO J. 1990 Mar;9(3):697–704. doi: 10.1002/j.1460-2075.1990.tb08162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Petersen C. C., Petersen O. H., Berridge M. J. The role of endoplasmic reticulum calcium pumps during cytosolic calcium spiking in pancreatic acinar cells. J Biol Chem. 1993 Oct 25;268(30):22262–22264. [PubMed] [Google Scholar]
- Petersen C. C., Toescu E. C., Petersen O. H. Different patterns of receptor-activated cytoplasmic Ca2+ oscillations in single pancreatic acinar cells: dependence on receptor type, agonist concentration and intracellular Ca2+ buffering. EMBO J. 1991 Mar;10(3):527–533. doi: 10.1002/j.1460-2075.1991.tb07979.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petersen C. C., Toescu E. C., Potter B. V., Petersen O. H. Inositol triphosphate produces different patterns of cytoplasmic Ca2+ spiking depending on its concentration. FEBS Lett. 1991 Nov 18;293(1-2):179–182. doi: 10.1016/0014-5793(91)81181-7. [DOI] [PubMed] [Google Scholar]
- Petersen O. H., Petersen C. C., Kasai H. Calcium and hormone action. Annu Rev Physiol. 1994;56:297–319. doi: 10.1146/annurev.ph.56.030194.001501. [DOI] [PubMed] [Google Scholar]
- Philpott H. G., Petersen O. H. Separate activation sites for cholecystokinin and bombesin on pancreatic acini: an electrophysiological study employing a competitive antagonist for the action of CCK. Pflugers Arch. 1979 Nov;382(3):263–267. doi: 10.1007/BF00583711. [DOI] [PubMed] [Google Scholar]
- Rousseau E., Smith J. S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol. 1987 Sep;253(3 Pt 1):C364–C368. doi: 10.1152/ajpcell.1987.253.3.C364. [DOI] [PubMed] [Google Scholar]
- Streb H., Heslop J. P., Irvine R. F., Schulz I., Berridge M. J. Relationship between secretagogue-induced Ca2+ release and inositol polyphosphate production in permeabilized pancreatic acinar cells. J Biol Chem. 1985 Jun 25;260(12):7309–7315. [PubMed] [Google Scholar]
- Thorn P., Lawrie A. M., Smith P. M., Gallacher D. V., Petersen O. H. Local and global cytosolic Ca2+ oscillations in exocrine cells evoked by agonists and inositol trisphosphate. Cell. 1993 Aug 27;74(4):661–668. doi: 10.1016/0092-8674(93)90513-p. [DOI] [PubMed] [Google Scholar]
- Thorn P., Petersen O. H. Activation of nonselective cation channels by physiological cholecystokinin concentrations in mouse pancreatic acinar cells. J Gen Physiol. 1992 Jul;100(1):11–25. doi: 10.1085/jgp.100.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thorn P., Petersen O. H. Calcium oscillations in pancreatic acinar cells, evoked by the cholecystokinin analogue JMV-180, depend on functional inositol 1,4,5-trisphosphate receptors. J Biol Chem. 1993 Nov 5;268(31):23219–23221. [PubMed] [Google Scholar]
- Wakui M., Osipchuk Y. V., Petersen O. H. Receptor-activated cytoplasmic Ca2+ spiking mediated by inositol trisphosphate is due to Ca2(+)-induced Ca2+ release. Cell. 1990 Nov 30;63(5):1025–1032. doi: 10.1016/0092-8674(90)90505-9. [DOI] [PubMed] [Google Scholar]
- Wakui M., Potter B. V., Petersen O. H. Pulsatile intracellular calcium release does not depend on fluctuations in inositol trisphosphate concentration. Nature. 1989 May 25;339(6222):317–320. doi: 10.1038/339317a0. [DOI] [PubMed] [Google Scholar]
- Yule D. I., Gallacher D. V. Oscillations of cytosolic calcium in single pancreatic acinar cells stimulated by acetylcholine. FEBS Lett. 1988 Nov 7;239(2):358–362. doi: 10.1016/0014-5793(88)80951-7. [DOI] [PubMed] [Google Scholar]