Presynaptic α4β2 nicotinic acetylcholine receptors increase glutamate release and serotonin neuron excitability in the dorsal raphe nucleus

Journal of Neuroscience

Volumn 32, Issue 43, 2012, Pages 15148-15157

  Garduño, Julieta ^a   Galindo Charles, Luis ^a   Jiménez Rodríguez, Javier ^a   Galarraga, Elvira ^b   Tapia, Dagoberto ^b   Mihailescu, Stefan ^a   Hernandez Lopez, Salvador ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; GLUTAMIC ACID; NICOTINIC RECEPTOR ALPHA4BETA2; SEROTONIN; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOCYTOCHEMISTRY; MALE; NERVE CELL EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACETYLCHOLINE; ACONITINE; ANIMALS; ANIMALS, NEWBORN; ATROPINE; BICUCULLINE; CADMIUM CHLORIDE; CHELATING AGENTS; CHOLINERGIC AGONISTS; DIHYDRO-BETA-ERYTHROIDINE; EGTAZIC ACID; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GLUTAMIC ACID; INDOLES; MALE; MUSCARINIC ANTAGONISTS; NICOTINE; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; PHYSOSTIGMINE; PRESYNAPTIC TERMINALS; RAPHE NUCLEI; RATS; RATS, WISTAR; RECEPTORS, NICOTINIC; RYANODINE; SEROTONERGIC NEURONS; SEROTONIN; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 84867815716     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0941-12.2012     Document Type: Article

References (67)

1. Alkondon M, Albuquerque EX (1995) Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. III. Agonist actions of the novel alkaloid epibatidine and analysis of type II current. J Pharmacol Exp Ther 274:771-782.
2. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371.
3. Bayliss DA, Li YW, Talley EM (1997) Effects of serotonin on caudal raphe neurons: inhibition of N and P/Q-type calcium channels and the afterhy-perpolarization. J Neurophysiol 77:1362-1374.
4. Beck SG, Pan YZ, Akanwa AC, Kirby LG (2004) Median and dorsal raphe neurons are not electrophysiologically identical. J Neurophysiol 91:994-1005.
5. Bitner RS, Nikkel AL (2002) Alpha-7 nicotinic receptor expression by two distinct cell types in the dorsal raphe nucleus and locus coeruleus of rat. Brain Res 938:45-54.
6. Bitner RS, Nikkel AL, Curzon P, Donnelly-Roberts DL, Puttfarcken PS, Namovic M, Jacobs IC, Meyer MD, Decker MW (2000) Reduced nico-tinic receptor-mediated antinociception following in vivo antisense knock-down in rat. Brain Res 871:66-74.
7. Brioni JD, O'Neill AB, Kim DJ, Buckley MJ, Decker MW, Arneric SP (1994) Anxiolytic-like effects of the novel cholinergic channel activator ABT-418. J Pharmacol Exp Ther 271:353-361.
8. Buisson B, Gopalakrishnan M, Arneric SP, Sullivan JP, Bertrand D (1996) Human alpha4beta2 neuronal nicotinic acetylcholine receptor in HEK 293 cells: a patch-clamp study. J Neurosci 16:7880-7891.
9. Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABAA, and glutamate receptors. J Neurosci 21:9917-9929.
10. Chang B, Daniele CA, Gallagher K, Madonia M, Mitchum RD, Barrett L, Vezina P, McGehee DS (2011) Nicotinic excitation of serotonergic projections from dorsal raphe to the nucleus accumbens. J Neurophysiol 106:801-808.
11. Cheeta S, Irvine EE, Kenny PJ, File SE (2001) The dorsal raphe nucleus is a crucial structure mediating nicotine's anxiolytic effects and the development of tolerance and withdrawal responses. Psycopharmacology (Berl) 155:78-85.
12. Commons KG (2008) Alpha4 containing nicotinic receptors are positioned to mediate postsynaptic effects on 5-HT neurons in the rat dorsal raphe nucleus. Neuroscience 153:851-859.
13. 2+ transients at the presynaptic terminal of a developing CNS inhibitory synapse. J Neurosci 24:6946-6957.
14. Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, Brussaard AB, Mansvelder HD (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54:73-87.
15. Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 25:317-324.
16. + stores. J Neurochem 81:606-614.
17. Dickinson JA, Kew JN, 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.
18. Engberg G, Erhardt S, Sharp T, Hajos M (2000) Nicotine inhibits firing activity of dorsal raphe 5-HT neurones in vivo. Naunyn Schmiedebergs Arch Pharmacol 362:41-45.
19. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of a4 and /32 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41:31-37.
20. + permeability of nicotinic acetylcholine receptors. Cell Calcium 35:1-8.
21. Galindo-Charles L, Hernandez-Lopez S, Galarraga E, Tapia D, Bargas J, Gar-duño J, Frías-Dominguez C, Drucker-Colin R, Mihailescu S (2008) Se-rotoninergic dorsal raphe neurons possess functional postsynaptic nicotinic acetylcholine receptors. Synapse 62:601-615.
22. Gioanni Y, Rougeot C, Clarke PB, Lepouse C, Thierry AM, Vidal C (1999) Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalamo-cortical transmission. Eur J Neurosci 11:18-30.
23. Girod R, Role LW (2001) Long-lasting enhancement of glutamatergic synaptic transmission by acetylcholine contrasts with response adaptation after exposure to low-level nicotine. J Neurosci 21:5182-5190.
24. Grahn RE, Watkins LR, Maier SF (2000) Impaired escape performance and enhanced conditioned fear in rats following exposure to an uncontrollable stressor are mediated by glutamate and nitric oxide in the dorsal raphe nucleus. Behav Brain Res 112:33-41.
25. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
26. Hogg RC, Raggenbass M, Bertrand D (2003) Nicotinic acetylcholine receptors: from structure to brain function. Rev Physiol Biochem Pharmacol 147:1-46.
27. Hsiao B, Dweck D, Luetje CW (2001) Subunit-dependent modulation of neuronal nicotinic receptors by zinc. J Neurosci 21:1848-1856.
28. Jensen AA, Frølund B, Liljefors T, Krogsgaard-Larsen P (2005) Neuronal nicotinic acetylcholine receptors: structural revelations, target identifications, and therapeutic inspirations. J Med Chem 48:4705-4745.
29. Jindrichova M, Lansdell SJ, Millar NS (2012) Changes in temperature have opposing effects on current amplitude in a7 and a4/32 nicotinic acetylcholine receptors. PLoS One 7:e32073.
30. Kawashima N, Karasawa J, Shimazaki T, Chaki S, Okuyama S, Yasuhara A, Nakazato A (2005) Neuropharmacological profiles of antagonists of group II metabotropic glutamate receptors. Neurosci Lett 378:131-134.
31. Kirby LG, Pan YZ, Freeman-Daniels E, Rani S, Nunan JD, Akanwa A, Beck SG (2007) Cellular effects of swim stress in the dorsal raphe nucleus. Psycho-neuroendocrinology 32:712-723.
32. Lambe EK, Picciotto MR, Aghajanian GK (2003) Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuro-psychopharmacology 28:216-225.
33. + ions in nicotinic facilitation of GABA release in mouse thalamus. J Neurosci 17:576-585.
34. Li X, Rainnie DG, McCarley RW, Greene RW (1998) Presynaptic nicotinic receptors facilitate monoaminergic transmission. JNeurosci 18:1904-1912.
35. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP, Marty A (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3:1256-1265.
36. Maggi L, Sola E, Minneci F, Le Magueresse C, Changeux JP, Cherubini E (2004) Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus. J Physiol 559:863-874.
37. Mansvelder HD, Keath JR, McGehee DS (2002) Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33:905-919.
38. Marinelli S, Schnell SA, Hack SP, Christie MJ, Wessendorf MW, Vaughan CW (2004) Serotonergic and nonserotonergic dorsal raphe neurons are pharmacologically and electrophysiologically heterogeneous. J Neuro-physiol 92:3532-3537.
39. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696.
40. Mihailescu S, Palomero-Rivero M, Meade-Huerta P, Maza-Flores A, Drucker-Colín R (1998) Effects of nicotine and mecamylamine on rat dorsal raphe neurons. Eur J Pharmacol 360:31-36.
41. Mihailescu S, Guzman-Marín R, Drucker-Colín R (2001) Nicotine stimulation of dorsal raphe neurons: effects on laterodorsal and pedunculopon-tine neurons. EurNeuropsychopharmacol 11:359-366.
42. Mihailescu S, Guzman-Marín R, Domínguezmdel C, Drucker-Colín R (2002) Mechanisms of nicotine actions on dorsal raphe serotoninergic neurons. Eur J Pharmacol 452:77-82.
43. Papke RL, Webster JC, Lippiello PM, Bencherif M, Francis MM (2000) The activation and inhibition of human nicotinic acetylcholine receptor by RJR-2403 indicate a selectivity for the alpha4beta2 receptor subtype. J Neurochem 75:204-216.
44. Paris JM, Cunningham KA (1994) Habenula lesions decrease the responsiveness of dorsal raphe serotonin neurons to cocaine. Pharmacol Biochem Behav 49:555-560.
45. Paul IA, Skolnick P (2003) Glutamate and depression: clinical and preclinical studies. Ann NY Acad Sci 1003:250-272.
46. 2+ current inhibition produced by serotonin in rat dorsal raphe neurons. JNeurosci 11:3594-3609.
47. Picciotto MR (2003) Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol Sci 24:493-499.
48. Rousseau SJ, Jones IW, Pullar IA, Wonnacott S (2005) Presynaptic alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate [H]D-aspartate release from rat frontal cortex in vitro. Neuropharmacology 49:59-72.
49. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
50. Seth P, Cheeta S, Tucci S, File SE (2002) Nicotinic-serotonergic interactions in brain and behaviour. Pharmacol Biochem Behav 71:795-805.
51. Sharma G, Vijayaraghavan S (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38:929-939.
52. 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.
53. Sher E, Chen Y, Sharples TJ, Broad LM, Benedetti G, Zwart R, McPhie GI, Pearson KH, Baldwinson T, De Filippi G (2004) Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr Top Med Chem 4:283-297.
54. Shoop RD, Chang KT, Ellisman MH, Berg DK (2001) Synaptically driven calcium transients via nicotinic receptors on somatic spines. J Neurosci 21:771-781.
55. Soiza-Reilly M, Commons KG (2011) Glutamatergic drive of the dorsal raphe nucleus. J Chem Neuroanat 41:247-255.
56. Trullas R, Skolnick P (1990) Functional antagonists at the NMDA receptor complex exhibit antidepressant actions. Eur J Pharmacol 185:1-10.
57. Tsuneki H, Klink R, Lena C, Korn H, Changeux JP (2000) Calcium mobilization elicited by two types of nicotinic acetylcholine receptors in mouse substantia nigra pars compacta. Eur J Neurosci 12:2475-2485.
58. Vandermaelen CP, Aghajanian GK (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extra-cellularly and intracellularly in rat brain slices. Brain Res 289:109-119.
59. Whiting PJ, Liu R, Morley BJ, Lindstrom JM (1987) Structurally different neuronal nicotinic acetylcholine receptor subtypes purified and characterized using monoclonal antibodies. J Neurosci 7:4005-4016.
60. Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92-98.
61. Woolf NJ, Butcher LL (1989) Cholinergic systems in the rat brain. IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 23:519-540.
62. Wooltorton JR, Pidoplichko VI, Broide RS, Dani JA (2003) Differential de-sensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23:3176-3185.
63. Wu J, Lukas RJ (2011) Naturally expressed nicotinic acetylcholine receptor subtypes. Biochem Pharmacol 82:800-807.
64. Yang K, Hu J, Lucero L, Liu Q, Zheng C, Zhen X, Jin G, Lukas RJ, Wu J (2009) Distinctive nicotinic acetylcholine receptor functional phenotypes of rat ventral tegmental area dopaminergic neurons. J Physiol 587:345-361.
65. Yilmaz A, Schulz D, Aksoy A, Canbeyli R (2002) Prolonged effect of an anesthetic dose of ketamine on behavioral despair. Pharmacol Biochem Behav 71:341-344.
66. Zoli M, Lena C, Picciotto MR, Changeux JP (1998) Identification of four classes of brain nicotinic receptors using /32 mutant mice. J Neurosci 18:4461-4472.
67. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.