Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 2003 Jul 15;373(Pt 2):313–318. doi: 10.1042/BJ20030472

Modulation of spontaneous transmitter release from the frog neuromuscular junction by interacting intracellular Ca(2+) stores: critical role for nicotinic acid-adenine dinucleotide phosphate (NAADP).

Eugen Brailoiu 1, Sandip Patel 1, Nae J Dun 1
PMCID: PMC1223519  PMID: 12749764

Abstract

Nicotinic acid-adenine dinucleotide phosphate (NAADP) is a recently described potent intracellular Ca(2+)-mobilizing messenger active in a wide range of diverse cell types. In the present study, we have investigated the interaction of NAADP with other Ca(2+)-mobilizing messengers in the release of transmitter at the frog neuromuscular junction. We show, for the first time, that NAADP enhances neurosecretion in response to inositol 1,4,5-trisphosphate (IP(3)), cADP-ribose (cADPR) and sphingosine 1-phosphate (S1P), but not sphingosylphosphorylcholine. Thapsigargin was without effect on transmitter release in response to NAADP, but blocked the responses to subsequent application of IP(3), cADPR and S1P and their potentiation by NAADP. Asynchronous neurotransmitter release may therefore involve functional coupling of endoplasmic reticulum Ca(2+) stores with distinct Ca(2+) stores targeted by NAADP.

Full Text

The Full Text of this article is available as a PDF (143.9 KB).

Selected References

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

  1. Bak J., White P., Timár G., Missiaen L., Genazzani A. A., Galione A. Nicotinic acid adenine dinucleotide phosphate triggers Ca2+ release from brain microsomes. Curr Biol. 1999 Jul 15;9(14):751–754. doi: 10.1016/s0960-9822(99)80335-2. [DOI] [PubMed] [Google Scholar]
  2. Berridge Georgina, Cramer Rainer, Galione Antony, Patel Sandip. Metabolism of the novel Ca2+-mobilizing messenger nicotinic acid-adenine dinucleotide phosphate via a 2'-specific Ca2+-dependent phosphatase. Biochem J. 2002 Jul 1;365(Pt 1):295–301. doi: 10.1042/BJ20020180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berridge Georgina, Dickinson George, Parrington John, Galione Antony, Patel Sandip. Solubilization of receptors for the novel Ca2+-mobilizing messenger, nicotinic acid adenine dinucleotide phosphate. J Biol Chem. 2002 Sep 9;277(46):43717–43723. doi: 10.1074/jbc.M203224200. [DOI] [PubMed] [Google Scholar]
  4. Berridge M. J., Lipp P., Bootman M. D. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000 Oct;1(1):11–21. doi: 10.1038/35036035. [DOI] [PubMed] [Google Scholar]
  5. Berridge M. J. Neuronal calcium signaling. Neuron. 1998 Jul;21(1):13–26. doi: 10.1016/s0896-6273(00)80510-3. [DOI] [PubMed] [Google Scholar]
  6. Boittin François-Xavier, Galione Antony, Evans A. Mark. Nicotinic acid adenine dinucleotide phosphate mediates Ca2+ signals and contraction in arterial smooth muscle via a two-pool mechanism. Circ Res. 2002 Dec 13;91(12):1168–1175. doi: 10.1161/01.res.0000047507.22487.85. [DOI] [PubMed] [Google Scholar]
  7. Brailoiu E., Miyamoto M. D., Dun N. J. Nicotinic acid adenine dinucleotide phosphate enhances quantal neurosecretion at the frog neuromuscular junction: possible action on synaptic vesicles in the releasable pool. Mol Pharmacol. 2001 Oct;60(4):718–724. [PubMed] [Google Scholar]
  8. Brailoiu E., Miyamoto M. D. Inositol trisphosphate and cyclic adenosine diphosphate-ribose increase quantal transmitter release at frog motor nerve terminals: possible involvement of smooth endoplasmic reticulum. Neuroscience. 2000;95(4):927–931. doi: 10.1016/s0306-4522(99)00509-6. [DOI] [PubMed] [Google Scholar]
  9. Brailoiu Eugen, Cooper Robin L., Dun Nae J. Sphingosine 1-phosphate enhances spontaneous transmitter release at the frog neuromuscular junction. Br J Pharmacol. 2002 Aug;136(8):1093–1097. doi: 10.1038/sj.bjp.0704839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brailoiu Eugen, Dun Nae J. Extra- and intracellular sphingosylphosphorylcholine promote spontaneous transmitter release from frog motor nerve endings. Mol Pharmacol. 2003 Jun;63(6):1430–1436. doi: 10.1124/mol.63.6.1430. [DOI] [PubMed] [Google Scholar]
  11. Burdakov D., Galione A. Two neuropeptides recruit different messenger pathways to evoke Ca2+ signals in the same cell. Curr Biol. 2000 Aug 24;10(16):993–996. doi: 10.1016/s0960-9822(00)00649-7. [DOI] [PubMed] [Google Scholar]
  12. Cancela J. M., Churchill G. C., Galione A. Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature. 1999 Mar 4;398(6722):74–76. doi: 10.1038/18032. [DOI] [PubMed] [Google Scholar]
  13. Cancela J. M., Gerasimenko O. V., Gerasimenko J. V., Tepikin A. V., Petersen O. H. Two different but converging messenger pathways to intracellular Ca(2+) release: the roles of nicotinic acid adenine dinucleotide phosphate, cyclic ADP-ribose and inositol trisphosphate. EMBO J. 2000 Jun 1;19(11):2549–2557. doi: 10.1093/emboj/19.11.2549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cancela Jose M., Van Coppenolle Fabien, Galione Antony, Tepikin Alexei V., Petersen Ole H. Transformation of local Ca2+ spikes to global Ca2+ transients: the combinatorial roles of multiple Ca2+ releasing messengers. EMBO J. 2002 Mar 1;21(5):909–919. doi: 10.1093/emboj/21.5.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cases I., de Lorenzo V. The black cat/white cat principle of signal integration in bacterial promoters. EMBO J. 2001 Jan 15;20(1-2):1–11. doi: 10.1093/emboj/20.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chameau P., Van de Vrede Y., Fossier P., Baux G. Ryanodine-, IP3- and NAADP-dependent calcium stores control acetylcholine release. Pflugers Arch. 2001 Nov;443(2):289–296. doi: 10.1007/s004240100691. [DOI] [PubMed] [Google Scholar]
  17. Churchill G. C., Galione A. Spatial control of Ca2+ signaling by nicotinic acid adenine dinucleotide phosphate diffusion and gradients. J Biol Chem. 2000 Dec 8;275(49):38687–38692. doi: 10.1074/jbc.M005827200. [DOI] [PubMed] [Google Scholar]
  18. Churchill Grant C., Okada Yuhei, Thomas Justyn M., Genazzani Armando A., Patel Sandip, Galione Antony. NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell. 2002 Nov 27;111(5):703–708. doi: 10.1016/s0092-8674(02)01082-6. [DOI] [PubMed] [Google Scholar]
  19. Copello J. A., Qi Y., Jeyakumar L. H., Ogunbunmi E., Fleischer S. Lack of effect of cADP-ribose and NAADP on the activity of skeletal muscle and heart ryanodine receptors. Cell Calcium. 2001 Oct;30(4):269–284. doi: 10.1054/ceca.2001.0235. [DOI] [PubMed] [Google Scholar]
  20. Fill Michael, Copello Julio A. Ryanodine receptor calcium release channels. Physiol Rev. 2002 Oct;82(4):893–922. doi: 10.1152/physrev.00013.2002. [DOI] [PubMed] [Google Scholar]
  21. Genazzani A. A., Galione A. Nicotinic acid-adenine dinucleotide phosphate mobilizes Ca2+ from a thapsigargin-insensitive pool. Biochem J. 1996 May 1;315(Pt 3):721–725. doi: 10.1042/bj3150721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Genazzani Armando A., Billington Richard A. NAADP: an atypical Ca2+-release messenger? Trends Pharmacol Sci. 2002 Apr;23(4):165–167. doi: 10.1016/s0165-6147(00)01990-8. [DOI] [PubMed] [Google Scholar]
  23. Guse Andreas H. Cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP): novel regulators of Ca2+-signaling and cell function. Curr Mol Med. 2002 May;2(3):273–282. doi: 10.2174/1566524024605707. [DOI] [PubMed] [Google Scholar]
  24. Hohenegger Martin, Suko Josef, Gscheidlinger Regina, Drobny Helmut, Zidar Andreas. Nicotinic acid-adenine dinucleotide phosphate activates the skeletal muscle ryanodine receptor. Biochem J. 2002 Oct 15;367(Pt 2):423–431. doi: 10.1042/BJ20020584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lee H. C., Aarhus R. A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J Biol Chem. 1995 Feb 3;270(5):2152–2157. doi: 10.1074/jbc.270.5.2152. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Meyer zu Heringdorf Dagmar, Himmel Herbert M., Jakobs Karl H. Sphingosylphosphorylcholine-biological functions and mechanisms of action. Biochim Biophys Acta. 2002 May 23;1582(1-3):178–189. doi: 10.1016/s1388-1981(02)00154-3. [DOI] [PubMed] [Google Scholar]
  28. Mitchell Kathryn J., Lai F. Anthony, Rutter Guy A. Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2+ release from insulin-containing vesicles in living pancreatic beta-cells (MIN6). J Biol Chem. 2003 Jan 21;278(13):11057–11064. doi: 10.1074/jbc.M210257200. [DOI] [PubMed] [Google Scholar]
  29. Mojzisová A., Krizanová O., Záciková L., Komínková V., Ondrias K. Effect of nicotinic acid adenine dinucleotide phosphate on ryanodine calcium release channel in heart. Pflugers Arch. 2001 Feb;441(5):674–677. doi: 10.1007/s004240000465. [DOI] [PubMed] [Google Scholar]
  30. Patel S., Churchill G. C., Galione A. Coordination of Ca2+ signalling by NAADP. Trends Biochem Sci. 2001 Aug;26(8):482–489. doi: 10.1016/s0968-0004(01)01896-5. [DOI] [PubMed] [Google Scholar]
  31. Patel S., Churchill G. C., Sharp T., Galione A. Widespread distribution of binding sites for the novel Ca2+-mobilizing messenger, nicotinic acid adenine dinucleotide phosphate, in the brain. J Biol Chem. 2000 Nov 24;275(47):36495–36497. doi: 10.1074/jbc.C000458200. [DOI] [PubMed] [Google Scholar]
  32. Patel S., Joseph S. K., Thomas A. P. Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium. 1999 Mar;25(3):247–264. doi: 10.1054/ceca.1999.0021. [DOI] [PubMed] [Google Scholar]
  33. Patel Sandip. NAADP on the up in pancreatic beta cells-a sweet message? Bioessays. 2003 May;25(5):430–433. doi: 10.1002/bies.10276. [DOI] [PubMed] [Google Scholar]
  34. Payne Shawn G., Milstien Sheldon, Spiegel Sarah. Sphingosine-1-phosphate: dual messenger functions. FEBS Lett. 2002 Oct 30;531(1):54–57. doi: 10.1016/s0014-5793(02)03480-4. [DOI] [PubMed] [Google Scholar]
  35. Silinsky E. M., Watanabe M., Redman R. S., Qiu R., Hirsh J. K., Hunt J. M., Solsona C. S., Alford S., MacDonald R. C. Neurotransmitter release evoked by nerve impulses without Ca2+ entry through Ca2+ channels in frog motor nerve endings. J Physiol. 1995 Feb 1;482(Pt 3):511–520. doi: 10.1113/jphysiol.1995.sp020536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Taylor C. W. Inositol trisphosphate receptors: Ca2+-modulated intracellular Ca2+ channels. Biochim Biophys Acta. 1998 Dec 8;1436(1-2):19–33. doi: 10.1016/s0005-2760(98)00122-2. [DOI] [PubMed] [Google Scholar]
  37. Young K. W., Nahorski S. R. Sphingosine 1-phosphate: a Ca2+ release mediator in the balance. Cell Calcium. 2002 Nov-Dec;32(5-6):335–341. doi: 10.1016/s0143416002001835. [DOI] [PubMed] [Google Scholar]

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

RESOURCES