cADP-ribose potentiates cytosolic Ca2+ elevation and Ca2+ entry via L-type voltage-activated Ca2+ channels in NG108-15 neuronal cells (original) (raw)

. 2000 Jan 15;345(Pt 2):207–215.

Abstract

The effects of cADP-ribose (cADPR), a metabolite of beta-NAD(+), on the elevation of cytoplasmic free Ca(2+) concentration ([Ca(2+)](i)) and Ca(2+) influx through voltage-activated Ca(2+) channels (VACCs) were studied in NG108-15 neuroblastomaxglioma hybrid cells. NG108-15 cells were pre-loaded with fura-2 and whole-cell patch-clamped. Application of cADPR through patch pipettes did not by itself trigger any [Ca(2+)](i) rise at the resting membrane potential. A rise in [Ca(2+)](i) was evoked upon sustained membrane depolarization, and was significantly larger in cADPR-infused cells than in non-infused cells. This potentiation in the [Ca(2+)](i) elevation was reproduced by infusion of beta-NAD(+), and was blocked by 8-bromo-cADPR and antagonized by external application of ryanodine or by pretreatment of cells with FK506. Nicotinamide inhibited beta-NAD(+)-induced, but not cADPR-elicited, potentiation. [Ca(2+)](i) increases or Ca(2+) influx, measured by Mn(2+) quenching, elicited by the same protocol of depolarization was blocked completely by nifedipine but not by omega-conotoxin. Ca(2+) influx in cADPR- or beta-NAD(+)-infused cells was steeper and greater than that in control cells, and was inhibited partly by ryanodine. In contrast, ryanodine accelerated Ca(2+) influx in non-infused cells. These results show that cADPR amplifies both depolarization-induced [Ca(2+)](i) increase and Ca(2+) influx through L-type VACCs. These results suggest that cADPR functions on ryanodine receptors as a direct agonist and also interacts with L-type VACCs as an indirect agonist, i.e. via a retrograde signal.

Full Text

The Full Text of this article is available as a PDF (212.8 KB).

Selected References

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

  1. Bennett D. L., Bootman M. D., Berridge M. J., Cheek T. R. Ca2+ entry into PC12 cells initiated by ryanodine receptors or inositol 1,4,5-trisphosphate receptors. Biochem J. 1998 Jan 15;329(Pt 2):349–357. doi: 10.1042/bj3290349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berridge M. J., Bootman M. D., Lipp P. Calcium--a life and death signal. Nature. 1998 Oct 15;395(6703):645–648. doi: 10.1038/27094. [DOI] [PubMed] [Google Scholar]
  3. Chavis P., Fagni L., Lansman J. B., Bockaert J. Functional coupling between ryanodine receptors and L-type calcium channels in neurons. Nature. 1996 Aug 22;382(6593):719–722. doi: 10.1038/382719a0. [DOI] [PubMed] [Google Scholar]
  4. Davies P. J., Ireland D. R., McLachlan E. M. Sources of Ca2+ for different Ca(2+)-activated K+ conductances in neurones of the rat superior cervical ganglion. J Physiol. 1996 Sep 1;495(Pt 2):353–366. doi: 10.1113/jphysiol.1996.sp021599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Deterre P., Gelman L., Gary-Gouy H., Arrieumerlou C., Berthelier V., Tixier J. M., Ktorza S., Goding J., Schmitt C., Bismuth G. Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1. Possible role in the recycling of nicotinamide adenine dinucleotide metabolites. J Immunol. 1996 Aug 15;157(4):1381–1388. [PubMed] [Google Scholar]
  6. Empson R. M., Galione A. Cyclic ADP-ribose enhances coupling between voltage-gated Ca2+ entry and intracellular Ca2+ release. J Biol Chem. 1997 Aug 22;272(34):20967–20970. doi: 10.1074/jbc.272.34.20967. [DOI] [PubMed] [Google Scholar]
  7. Furuichi T., Furutama D., Hakamata Y., Nakai J., Takeshima H., Mikoshiba K. Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. J Neurosci. 1994 Aug;14(8):4794–4805. doi: 10.1523/JNEUROSCI.14-08-04794.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Giannini G., Conti A., Mammarella S., Scrobogna M., Sorrentino V. The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J Cell Biol. 1995 Mar;128(5):893–904. doi: 10.1083/jcb.128.5.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gray P. C., Johnson B. D., Westenbroek R. E., Hays L. G., Yates J. R., 3rd, Scheuer T., Catterall W. A., Murphy B. J. Primary structure and function of an A kinase anchoring protein associated with calcium channels. Neuron. 1998 May;20(5):1017–1026. doi: 10.1016/s0896-6273(00)80482-1. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Hashii M., Nakashima S., Yokoyama S., Enomoto K., Minabe Y., Nozawa Y., Higashida H. Bradykinin B2 receptor-induced and inositol tetrakisphosphate-evoked Ca2+ entry is sensitive to a protein tyrosine phosphorylation inhibitor in ras-transformed NIH/3T3 fibroblasts. Biochem J. 1996 Oct 15;319(Pt 2):649–656. doi: 10.1042/bj3190649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Higashida H., Hashii M., Fukuda K., Caulfield M. P., Numa S., Brown D. A. Selective coupling of different muscarinic acetylcholine receptors to neuronal calcium currents in DNA-transfected cells. Proc Biol Sci. 1990 Oct 22;242(1303):68–74. doi: 10.1098/rspb.1990.0105. [DOI] [PubMed] [Google Scholar]
  13. Higashida H., Robbins J., Egorova A., Noda M., Taketo M., Ishizaka N., Takasawa S., Okamoto H., Brown D. A. Nicotinamide-adenine dinucleotide regulates muscarinic receptor-coupled K+ (M) channels in rodent NG108-15 cells. J Physiol. 1995 Jan 15;482(Pt 2):317–323. doi: 10.1113/jphysiol.1995.sp020520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Higashida H., Yokoyama S., Hashii M., Taketo M., Higashida M., Takayasu T., Ohshima T., Takasawa S., Okamoto H., Noda M. Muscarinic receptor-mediated dual regulation of ADP-ribosyl cyclase in NG108-15 neuronal cell membranes. J Biol Chem. 1997 Dec 12;272(50):31272–31277. doi: 10.1074/jbc.272.50.31272. [DOI] [PubMed] [Google Scholar]
  15. Hua S. Y., Tokimasa T., Takasawa S., Furuya Y., Nohmi M., Okamoto H., Kuba K. Cyclic ADP-ribose modulates Ca2+ release channels for activation by physiological Ca2+ entry in bullfrog sympathetic neurons. Neuron. 1994 May;12(5):1073–1079. doi: 10.1016/0896-6273(94)90315-8. [DOI] [PubMed] [Google Scholar]
  16. Jeyakumar L. H., Copello J. A., O'Malley A. M., Wu G. M., Grassucci R., Wagenknecht T., Fleischer S. Purification and characterization of ryanodine receptor 3 from mammalian tissue. J Biol Chem. 1998 Jun 26;273(26):16011–16020. doi: 10.1074/jbc.273.26.16011. [DOI] [PubMed] [Google Scholar]
  17. Kano M., Garaschuk O., Verkhratsky A., Konnerth A. Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurones. J Physiol. 1995 Aug 15;487(1):1–16. doi: 10.1113/jphysiol.1995.sp020857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kasai H., Neher E. Dihydropyridine-sensitive and omega-conotoxin-sensitive calcium channels in a mammalian neuroblastoma-glioma cell line. J Physiol. 1992 Mar;448:161–188. doi: 10.1113/jphysiol.1992.sp019035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kino T., Hatanaka H., Hashimoto M., Nishiyama M., Goto T., Okuhara M., Kohsaka M., Aoki H., Imanaka H. FK-506, a novel immunosuppressant isolated from a Streptomyces. I. Fermentation, isolation, and physico-chemical and biological characteristics. J Antibiot (Tokyo) 1987 Sep;40(9):1249–1255. doi: 10.7164/antibiotics.40.1249. [DOI] [PubMed] [Google Scholar]
  20. Lee H. C. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol Rev. 1997 Oct;77(4):1133–1164. doi: 10.1152/physrev.1997.77.4.1133. [DOI] [PubMed] [Google Scholar]
  21. Lee H. C. Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J Biol Chem. 1993 Jan 5;268(1):293–299. [PubMed] [Google Scholar]
  22. 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]
  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. Morita K., Kitayama S., Dohi T. Stimulation of cyclic ADP-ribose synthesis by acetylcholine and its role in catecholamine release in bovine adrenal chromaffin cells. J Biol Chem. 1997 Aug 22;272(34):21002–21009. doi: 10.1074/jbc.272.34.21002. [DOI] [PubMed] [Google Scholar]
  25. Morrissette J., Heisermann G., Cleary J., Ruoho A., Coronado R. Cyclic ADP-ribose induced Ca2+ release in rabbit skeletal muscle sarcoplasmic reticulum. FEBS Lett. 1993 Sep 20;330(3):270–274. doi: 10.1016/0014-5793(93)80886-y. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Nakai J., Dirksen R. T., Nguyen H. T., Pessah I. N., Beam K. G., Allen P. D. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature. 1996 Mar 7;380(6569):72–75. doi: 10.1038/380072a0. [DOI] [PubMed] [Google Scholar]
  28. Noguchi N., Takasawa S., Nata K., Tohgo A., Kato I., Ikehata F., Yonekura H., Okamoto H. Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J Biol Chem. 1997 Feb 7;272(6):3133–3136. doi: 10.1074/jbc.272.6.3133. [DOI] [PubMed] [Google Scholar]
  29. Ogura A., Myojo Y., Higashida H. Bradykinin-evoked acetylcholine release via inositol trisphosphate-dependent elevation in free calcium in neuroblastoma x glioma hybrid NG108-15 cells. J Biol Chem. 1990 Feb 25;265(6):3577–3584. [PubMed] [Google Scholar]
  30. Sethi J. K., Empson R. M., Galione A. Nicotinamide inhibits cyclic ADP-ribose-mediated calcium signalling in sea urchin eggs. Biochem J. 1996 Oct 15;319(Pt 2):613–617. doi: 10.1042/bj3190613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sitsapesan R., McGarry S. J., Williams A. J. Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release. Trends Pharmacol Sci. 1995 Nov;16(11):386–391. doi: 10.1016/s0165-6147(00)89080-x. [DOI] [PubMed] [Google Scholar]
  32. Sonnleitner A., Conti A., Bertocchini F., Schindler H., Sorrentino V. Functional properties of the ryanodine receptor type 3 (RyR3) Ca2+ release channel. EMBO J. 1998 May 15;17(10):2790–2798. doi: 10.1093/emboj/17.10.2790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Timerman A. P., Onoue H., Xin H. B., Barg S., Copello J., Wiederrecht G., Fleischer S. Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J Biol Chem. 1996 Aug 23;271(34):20385–20391. doi: 10.1074/jbc.271.34.20385. [DOI] [PubMed] [Google Scholar]
  34. Walseth T. F., Lee H. C. Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochim Biophys Acta. 1993 Sep 13;1178(3):235–242. doi: 10.1016/0167-4889(93)90199-y. [DOI] [PubMed] [Google Scholar]