Nicotine-induced and depolarisation-induced glutamate release from hippocampus mossy fibre synaptosomes: Two distinct mechanisms

Journal of Neurochemistry

Volumn 110, Issue 2, 2009, Pages 570-580

  Bancila, Victor ^b,c   Cordeiro, J Miguel ^b   Bloc, Alain ^b   Dunant, Yves ^a,b  

^a Center Médical Universitaire   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Division of Anaesthesiology   (Switzerland)

Author keywords

Calcium; Glutamate release; Hippocampus mossy fibres; Membrane potential; Nicotine; Vesicular proton gradient

Indexed keywords

GLUTAMIC ACID; NICOTINE; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; COMPARATIVE STUDY; CONTROLLED STUDY; DEPOLARIZATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MALE; NERVE FIBER MEMBRANE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRIMARY AFFERENT DEPOLARIZATION; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

ANIMALS; CELL POLARITY; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MEMBRANE POTENTIALS; MOSSY FIBERS, HIPPOCAMPAL; NICOTINE; RATS; RATS, WISTAR; RECEPTORS, NICOTINIC; SYNAPTOSOMES;

RATTUS;

EID: 67649511966     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06169.x     Document Type: Article

References (41)

1. Amaral D. G. Dent J. A. (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195, 51 86. (Pubitemid 11098807)
2. Bancila V., Bloc A. Dunant Y. (2004a) Nicotine induces glutamate release from hippocampal mossy fibre synaptosomes, in Cholinergic Mechanisms, Function and Dysfunction (Silman I., Soreq H., Anglister L., Michaelson M. Fischer A., eds), pp. 456 461. Martin Dunitz, London.
3. Bancila V., Nikonenko I., Dunant Y. Bloc A. (2004b) Zinc inhibits glutamate release via activation of pre-synaptic K channels and reduces ischaemic damage in rat hippocampus. J. Neurochem. 90, 1243 1250. (Pubitemid 39167357)
4. Bennett M. R. (1995) The origin of Gaussian distributions of synaptic potentials. Prog. Neurobiol. 46, 331 350.
5. Blaustein M. P. Goldring J. M. (1975) Membrane potentials in pinched-off presynaptic nerve terminals monitored with a fluorescent probe: evidence that synaptosomes have potassium diffusion potentials. J. Physiol. Lond. 247, 589 615.
6. Bloedel J., Gage P. W., Llinas R. Quastel D. M. (1966) Transmitter release at the squid giant synapse in the presence of tetrodotoxin. Nature 212, 49 50.
7. Cordeiro J. M., Bancila V., Bloc A., Gonçalves P. P. Dunant Y. (2004) A calcium-proton antiport in presynaptic nerve terminals, in Cholinergic Mechanisms, Function and Dysfunction (Silman I., Soreq H., Anglister L., Michaelson M. Fischer A., eds), pp. 527 529. Martin Dunitz, London.
8. Dajas-Bailador F. Wonnacott S. (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol. Sci. 25, 317 324. (Pubitemid 38692424)
9. Dani J. A. Bertrand D. (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47, 699 729. (Pubitemid 46272144)
10. Descarries L., Gisiger V. Steriade M. (1997) Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol. 53, 603 625. (Pubitemid 27489823)
11. Dickinson J. A., Kew J. N. Wonnacott S. (2008) Presynaptic alpha 7- and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol. Pharmacol. 74, 348 359.
12. Dunant Y. Israël M. (2000) Neurotransmitter release in rapid synapses. Biochimie 82, 289 302. (Pubitemid 30391908)
13. + antiport in rapid neurotransmission. Ann. NY Acad. Sci. 1152, 100 112.
14. Falk-Vairant J., Corrèges P., Eder-Colli L. et al. (1996) Quantal acetylcholine release induced by mediatophore transfection. Proc. Natl Acad. Sci. USA 93, 5203 5207. (Pubitemid 26159426)
15. Fosse V. M., Kolstad J. Fonnum F. (1986) A bioluminescence method for the measurement of L-glutamate: applications to the study of changes in the release of L-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. J. Neurochem. 47, 340 349. (Pubitemid 16052846)
16. Girod R., Corrèges P., Jacquet J. Dunant Y. (1993) Space and time characteristics of transmitter release at the nerve-electroplaque junction of Torpedo. J. Physiol. Lond. 471, 129 157. (Pubitemid 23345574)
17. Girod R., Barazangi N., McGehee D. Role L. W. (2000) Facilitation of glutamatergic neurotransmission by presynaptic nicotinic acetylcholine receptors. Neuropharmacology 39, 2715 2725. (Pubitemid 30753043)
18. +-Antiport activity in synaptic vesicles isolated from sheep brain cortex. Neurosci. Lett. 247, 87 90. (Pubitemid 28240103)
19. Gonçalves P. P., Meireles S. M., Neves P. Vale M. G. (2000) Distinction between Ca(2+) pump and Ca(2+)/H(+) antiport activities in synaptic vesicles of sheep brain cortex. Neurochem. Int. 37, 387 396. (Pubitemid 30301731)
20. Gray R., Rajan A. S., Radcliffe K. A., Yakehiro M. Dani J. A. (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383, 713 716. (Pubitemid 26360646)
21. Helme-Guizon A., Davis S., Israel M., Lesbats B., Mallet J., Laroche S. Hicks A. (1998) Increase in syntaxin 1B and glutamate release in mossy fibre terminals following induction of LTP in the dentate gyrus: a candidate molecular mechanism underlying transsynaptic plasticity. Eur. J. Neurosci. 10, 2231 2237. (Pubitemid 28302325)
22. Israël M. Whittaker V. P. (1965) The isolation of mossy fibre endings from the granular layer of the cerebellar cortex. Experientia 21, 325 326.
23. Israël M., Lesbats B. Bruner J. (1993) Glutamate and acetylcholine release from cholinergic nerve terminals, a calcium control of the specificity of the release mechanism. Neurochem. Int. 22, 53 58.
24. Jonas P., Major G. Sakmann B. (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 472, 615 663. (Pubitemid 24015024)
25. Katz B. Miledi R. (1966) Input-output relation of a single synapse. Nature 212, 1242 1245.
26. Katz B. Miledi R. B. (1981) Does the motor nerve impulse evoke 'non-quantal' transmitter release? Proc. R. Soc. Lond. B 212, 131 137. (Pubitemid 11069397)
27. Kuno M., Turkanis S. A. Weakly J. N. (1971) Correlation between nerve terminal size and transmitter release at the neuromuscular junction of the frog. J, Physiol, Lond. 213, 545 556.
28. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39, 327 341. (Pubitemid 36897553)
29. 2+ ions in nicotinic facilitation of GABA release in mouse thalamus. J. Neurosci. 17, 576 585. (Pubitemid 27024570)
30. Lendvai B. Vizi E. S. (2008) Nonsynaptic chemical transmission through nicotinic acetylcholine receptors. Physiol. Rev. 88, 333 349.
31. Lopez E., Arce C., Vicente S., Oset-Gasque M. J. Gonzalez M. P. (2001) Nicotinic receptors mediate the release of amino acid neurotransmitters in cultured cortical neurons. Cereb. Cortex 11, 158 163. (Pubitemid 32095138)
32. Meunier F. M. (1984) Relationship between presynaptic membrane potential and acetylcholine release in synaptosomes from Torpedo electric organ. J, Physiol, Lond. 354, 121 137.
33. Petersen O. H. Tepikin A. V. (2008) Polarized calcium signaling in exocrine gland cells. Annu. Rev. Physiol. 70, 273 299. (Pubitemid 351738181)
34. Raiteri L., Stigliani S., Zedda L., Raiteri M. Bonanno G. (2002) Multiple mechanisms of transmitter release evoked by 'pathologically' elevated extracellular [K+]: involvement of transporter reversal and mitochondrial calcium. J. Neurochem. 80, 706 714. (Pubitemid 34809978)
35. Role L. W. Berg D. K. (1996) Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16, 1077 1085. (Pubitemid 26227229)
36. Sharma G. Vijayaraghavan S. (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38, 929 939. (Pubitemid 36789765)
37. Sharma G., Grybko M. Vijayaraghavan S. (2008) Action potential- independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J. Neurosci. 28, 2563 2575. (Pubitemid 351348186)
38. Vogt K. E. Regehr W. G. (2001) Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J. Neurosci. 21, 75 83. (Pubitemid 32098728)
39. 2+/calmodulin signaling pathway in rat prefrontal cortex nerve terminals. Synapse 59, 491 501.
40. Wonnacott S. (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci. 20, 92 98. (Pubitemid 27050704)
41. Zoccarato F., Cavallini L. Alexandre A. (1999) The pH-sensitive dye acridine orange as a tool to monitor exocytosis/endocytosis in synaptosomes. J. Neurochem. 72, 625 633. (Pubitemid 29055224)