Abstract
The effects of intracellular application of two novel Ca2+ releasing agents have been studied in cultured rat dorsal root ganglion (DRG) neurones by monitoring Ca(2+)-dependent currents as a physiological index of raised free cytosolic Ca2+ ([Ca2+]i). A protein based sperm factor (SF) extracted from mammalian sperm, has been found to trigger Ca2+ oscillations and to sensitize unfertilized mammalian eggs to calcium induced calcium release (CICR). In this study intracellular application of SF activated Ca(2+)-dependent currents in approximately two-thirds of DRG neurones. The SF induced activity was abolished by heat treatment, attenuated by increasing the intracellular Ca2+ buffering capacity of the cells and persisted when extracellular Ca2+ was replaced by Ba2+. In addition, activity could be triggered or potentiated by loading the cells with Ca2+ by activating a series of voltage-gated Ca2+ currents. Ca(2+)-activated inward current activity was also generated by intracellular application of cyclic ADP-ribose (cADPR), a metabolite of NAD+, which causes Ca2+ release in sea urchin eggs. This activity could also be enhanced by loading the cells with Ca2+. The cADPR induced activity, but not the SF induced activity, was abolished by depleting the caffeine sensitive Ca2+ store. Ruthenium red markedly attenuated SF induced activity but had little action on cADPR induced activity or caffeine induced activity. Our results indicate that both SF and cADPR release intracellular Ca2+ pools in DRG neurones and that they appear to act on subtly distinct stores or distinct intracellular Ca2+ release mechanisms, possibly by modulating CICR.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Berridge M. J. Cytoplasmic calcium oscillations: a two pool model. Cell Calcium. 1991 Feb-Mar;12(2-3):63–72. doi: 10.1016/0143-4160(91)90009-4. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Blaustein M. P. Calcium transport and buffering in neurons. Trends Neurosci. 1988 Oct;11(10):438–443. doi: 10.1016/0166-2236(88)90195-6. [DOI] [PubMed] [Google Scholar]
- Brorson J. R., Bleakman D., Gibbons S. J., Miller R. J. The properties of intracellular calcium stores in cultured rat cerebellar neurons. J Neurosci. 1991 Dec;11(12):4024–4043. doi: 10.1523/JNEUROSCI.11-12-04024.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Currie K. P., Scott R. H. Calcium-activated currents in cultured neurones from rat dorsal root ganglia. Br J Pharmacol. 1992 Jul;106(3):593–602. doi: 10.1111/j.1476-5381.1992.tb14381.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cuthbertson K. S., Cobbold P. H. Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+. Nature. 1985 Aug 8;316(6028):541–542. doi: 10.1038/316541a0. [DOI] [PubMed] [Google Scholar]
- Dale B., DeFelice L. J., Ehrenstein G. Injection of a soluble sperm fraction into sea-urchin eggs triggers the cortical reaction. Experientia. 1985 Aug 15;41(8):1068–1070. doi: 10.1007/BF01952148. [DOI] [PubMed] [Google Scholar]
- Dale B. Primary and secondary messengers in the activation of ascidian eggs. Exp Cell Res. 1988 Jul;177(1):205–211. doi: 10.1016/0014-4827(88)90038-9. [DOI] [PubMed] [Google Scholar]
- Dargie P. J., Agre M. C., Lee H. C. Comparison of Ca2+ mobilizing activities of cyclic ADP-ribose and inositol trisphosphate. Cell Regul. 1990 Feb;1(3):279–290. doi: 10.1091/mbc.1.3.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dupont G., Berridge M. J., Goldbeter A. Signal-induced Ca2+ oscillations: properties of a model based on Ca(2+)-induced Ca2+ release. Cell Calcium. 1991 Feb-Mar;12(2-3):73–85. doi: 10.1016/0143-4160(91)90010-c. [DOI] [PubMed] [Google Scholar]
- Ferris C. D., Snyder S. H. Inositol 1,4,5-trisphosphate-activated calcium channels. Annu Rev Physiol. 1992;54:469–488. doi: 10.1146/annurev.ph.54.030192.002345. [DOI] [PubMed] [Google Scholar]
- 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]
- Galione A. Ca(2+)-induced Ca2+ release and its modulation by cyclic ADP-ribose. Trends Pharmacol Sci. 1992 Aug;13(8):304–306. doi: 10.1016/0165-6147(92)90096-o. [DOI] [PubMed] [Google Scholar]
- Galione A., Lee H. C., Busa W. B. Ca(2+)-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science. 1991 Sep 6;253(5024):1143–1146. doi: 10.1126/science.1909457. [DOI] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Hellmich M. R., Strumwasser F. Purification and characterization of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul. 1991 Mar;2(3):193–202. doi: 10.1091/mbc.2.3.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holliday J., Adams R. J., Sejnowski T. J., Spitzer N. C. Calcium-induced release of calcium regulates differentiation of cultured spinal neurons. Neuron. 1991 Nov;7(5):787–796. doi: 10.1016/0896-6273(91)90281-4. [DOI] [PubMed] [Google Scholar]
- Jaffe L. F. Sources of calcium in egg activation: a review and hypothesis. Dev Biol. 1983 Oct;99(2):265–276. doi: 10.1016/0012-1606(83)90276-2. [DOI] [PubMed] [Google Scholar]
- Kennedy M. B. Regulation of neuronal function by calcium. Trends Neurosci. 1989 Nov;12(11):417–420. doi: 10.1016/0166-2236(89)90089-1. [DOI] [PubMed] [Google Scholar]
- Koshiyama H., Lee H. C., Tashjian A. H., Jr Novel mechanism of intracellular calcium release in pituitary cells. J Biol Chem. 1991 Sep 15;266(26):16985–16988. [PubMed] [Google Scholar]
- Kuba K. Release of calcium ions linked to the activation of potassium conductance in a caffeine-treated sympathetic neurone. J Physiol. 1980 Jan;298:251–269. doi: 10.1113/jphysiol.1980.sp013079. [DOI] [PMC free article] [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]
- 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]
- Lee H. C., Aarhus R. ADP-ribosyl cyclase: an enzyme that cyclizes NAD+ into a calcium-mobilizing metabolite. Cell Regul. 1991 Mar;2(3):203–209. doi: 10.1091/mbc.2.3.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee H. C. Specific binding of cyclic ADP-ribose to calcium-storing microsomes from sea urchin eggs. J Biol Chem. 1991 Feb 5;266(4):2276–2281. [PubMed] [Google Scholar]
- Lee H. C., Walseth T. F., Bratt G. T., Hayes R. N., Clapper D. L. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J Biol Chem. 1989 Jan 25;264(3):1608–1615. [PubMed] [Google Scholar]
- 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]
- Marrion N. V., Adams P. R. Release of intracellular calcium and modulation of membrane currents by caffeine in bull-frog sympathetic neurones. J Physiol. 1992 Jan;445:515–535. doi: 10.1113/jphysiol.1992.sp018937. [DOI] [PMC free article] [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]
- 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]
- Miller R. J. The control of neuronal Ca2+ homeostasis. Prog Neurobiol. 1991;37(3):255–285. doi: 10.1016/0301-0082(91)90028-y. [DOI] [PubMed] [Google Scholar]
- Miyazaki S. Repetitive calcium transients in hamster oocytes. Cell Calcium. 1991 Feb-Mar;12(2-3):205–216. doi: 10.1016/0143-4160(91)90021-6. [DOI] [PubMed] [Google Scholar]
- Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
- Nakagawa T., Okano H., Furuichi T., Aruga J., Mikoshiba K. The subtypes of the mouse inositol 1,4,5-trisphosphate receptor are expressed in a tissue-specific and developmentally specific manner. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6244–6248. doi: 10.1073/pnas.88.14.6244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otsu K., Willard H. F., Khanna V. K., Zorzato F., Green N. M., MacLennan D. H. Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem. 1990 Aug 15;265(23):13472–13483. [PubMed] [Google Scholar]
- Penner R., Neher E., Takeshima H., Nishimura S., Numa S. Functional expression of the calcium release channel from skeletal muscle ryanodine receptor cDNA. FEBS Lett. 1989 Dec 18;259(1):217–221. doi: 10.1016/0014-5793(89)81532-7. [DOI] [PubMed] [Google Scholar]
- Rusinko N., Lee H. C. Widespread occurrence in animal tissues of an enzyme catalyzing the conversion of NAD+ into a cyclic metabolite with intracellular Ca2+-mobilizing activity. J Biol Chem. 1989 Jul 15;264(20):11725–11731. [PubMed] [Google Scholar]
- Sah P., McLachlan E. M. Ca(2+)-activated K+ currents underlying the afterhyperpolarization in guinea pig vagal neurons: a role for Ca(2+)-activated Ca2+ release. Neuron. 1991 Aug;7(2):257–264. doi: 10.1016/0896-6273(91)90264-z. [DOI] [PubMed] [Google Scholar]
- Scott R. H., Pearson H. A., Dolphin A. C. Aspects of vertebrate neuronal voltage-activated calcium currents and their regulation. Prog Neurobiol. 1991;36(6):485–520. doi: 10.1016/0301-0082(91)90014-r. [DOI] [PubMed] [Google Scholar]
- Shoshan-Barmatz V., Pressley T. A., Higham S., Kraus-Friedmann N. Characterization of high-affinity ryanodine-binding sites of rat liver endoplasmic reticulum. Differences between liver and skeletal muscle. Biochem J. 1991 May 15;276(Pt 1):41–46. doi: 10.1042/bj2760041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stice S. L., Robl J. M. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol Reprod Dev. 1990 Mar;25(3):272–280. doi: 10.1002/mrd.1080250309. [DOI] [PubMed] [Google Scholar]
- Supattapone S., Worley P. F., Baraban J. M., Snyder S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem. 1988 Jan 25;263(3):1530–1534. [PubMed] [Google Scholar]
- Swann K. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development. 1990 Dec;110(4):1295–1302. doi: 10.1242/dev.110.4.1295. [DOI] [PubMed] [Google Scholar]
- Swann K. Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem J. 1992 Oct 1;287(Pt 1):79–84. doi: 10.1042/bj2870079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swann K., Whitaker M. J. Second messengers at fertilization in sea-urchin eggs. J Reprod Fertil Suppl. 1990;42:141–153. [PubMed] [Google Scholar]
- Thayer S. A., Perney T. M., Miller R. J. Regulation of calcium homeostasis in sensory neurons by bradykinin. J Neurosci. 1988 Nov;8(11):4089–4097. doi: 10.1523/JNEUROSCI.08-11-04089.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Walseth T. F., Aarhus R., Zeleznikar R. J., Jr, Lee H. C. Determination of endogenous levels of cyclic ADP-ribose in rat tissues. Biochim Biophys Acta. 1991 Aug 13;1094(1):113–120. doi: 10.1016/0167-4889(91)90032-s. [DOI] [PubMed] [Google Scholar]
- Walton P. D., Airey J. A., Sutko J. L., Beck C. F., Mignery G. A., Südhof T. C., Deerinck T. J., Ellisman M. H. Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J Cell Biol. 1991 Jun;113(5):1145–1157. doi: 10.1083/jcb.113.5.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wangemann P., Wittner M., Di Stefano A., Englert H. C., Lang H. J., Schlatter E., Greger R. Cl(-)-channel blockers in the thick ascending limb of the loop of Henle. Structure activity relationship. Pflugers Arch. 1986;407 (Suppl 2):S128–S141. doi: 10.1007/BF00584942. [DOI] [PubMed] [Google Scholar]