Effects of nicotine in the dopaminergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholine receptors

European Journal of Neuroscience

Volumn 17, Issue 7, 2003, Pages 1329-1337

  Marubio, L M ^a,b   Gardier, A M ^c   Durier, S ^c   David, D ^c   Klink, R ^a   Arroyo Jimenez, M M ^a   McIntosh, J M ^d   Rossi, F ^a   Champtiaux, N ^a   Zoli, M ^e   Changeux, J P ^a  

^a INSTITUT PASTEUR   (France)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Cocaine; Dopamine; Dopaminergic system; Locomotor activity; Microdialysis; Nicotine; Nicotinic acetylcholine receptor

Indexed keywords

ALPHA CONOTOXIN MII; ALPHA4 NICOTINIC ACETYLCHOLINE RECEPTOR; ALPHA6 NICOTINIC ACETYLCHOLINE RECEPTOR; BETA2 NICOTINIC ACETYLCHOLINE RECEPTOR; CONOTOXIN; IODINE 125; NICOTINE; NICOTINIC RECEPTOR; POTASSIUM CHLORIDE; UNCLASSIFIED DRUG;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; FEMALE; ISOTOPE LABELING; LOCOMOTION; MALE; MICRODIALYSIS; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SUBSTANTIA NIGRA; WILD TYPE;

ANIMALS; AUTORADIOGRAPHY; BICYCLO COMPOUNDS, HETEROCYCLIC; BINDING SITES; CONOTOXINS; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR SPACE; IODINE ISOTOPES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRODIALYSIS; MOTOR ACTIVITY; MUTAGENESIS; NEURAL NETWORKS (COMPUTER); NICOTINE; NICOTINIC AGONISTS; PATCH-CLAMP TECHNIQUES; PYRIDINES; RECEPTORS, NICOTINIC; SUBSTANTIA NIGRA; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 0038367987     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02564.x     Document Type: Article

References (46)

1. Alkondon, M. & Albuquerque, E.X. (1993) Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J. Pharmacol. Exp. Therap., 265, 1455-1473.
2. Arroyo-Jimenez, M.M., Bourgeois, J.P., Marubio, L.M., Le Sourd, A.M., Ottersen, O.P., Rinvik, E., Fairen, A. & Changeux, J.P. (1999) Ultrastructural localization of the alpha4-subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra. J. Neurosci., 19, 6475-6487.
3. Bevan, M.D. & Bolam, J.P. (1995) Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J. Neurosci., 15, 7105-7120.
4. Blaha, C.D., Allen, L.F., Das, S., Inglis, W.L., Latimer, M.P., Vincent, S.R. & Winn, P. (1996) Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats. J. Neurosci., 16, 714-722.
5. Cartier, G.E., Yoshikami, D., Gray, W.R., Luo, S., Olivera, B.M. & McIntosh, J.M. (1996) A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors. J. Biol. Chem., 271, 7522-7528.
6. Champtiaux, N., Zhi-Yan, H., Bessis, A., Rossi, F., Zoli, M., Marubio, L.M., McIntosh, J.M. & Changeux, J.P. (2002) Distribution and pharmacology of alpha6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J. Neurosci., 22, 1208-1217.
7. Clarke, P.B., Fu, D.S., Jakubovic, A. & Fibiger, H.C. (1988) Evidence that mesolimbic dopaminergic activation underlies the locomotor stimulant action of nicotine in rats. J. Pharmacol. Exp. Therap., 246, 701-708.
8. 125I-α-bungarotoxin. J. Neurosci., 5, 1307-1315.
9. Corrigall, W.A. & Coen, K.M. (1991) Selective dopamine antagonists reduce nicotine self-administration. Psychopharmacology, 104, 171-176.
10. Corrigall, W.A., Cohen, K.M. & Adamson, K.L. (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res., 653, 278-284.
11. Corrigall, W.A., Franklin, K.B.J., Cohen, K.M. & Clarke, P.B.S. (1992) The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology, 107, 285-289.
12. Forster, G.L. & Blaha, C.D. (2000) Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur J. Neurosci., 12, 3596-3604.
13. Franklin, K.B. & Paxinos, G. (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press. Toronto/San Diego.
14. Gerzanich, V., Kuryatov, A., Anand, R. & Lindstrom, J. (1997) 'Orphan' alpha6 nicotinic AChR subunit can form a functional heteromeric acetylcholine receptor. Mol Pharmacol., 51, 320-327.
15. Grady, S., Marks, M.J., Wonnacott, S. & Collins, A.C. (1992) Characterization of nicotinic receptor-mediated [3H]dopamine release from synaptosomes prepared from mouse striatum. J. Neurochem., 59, 848-856.
16. Groot-Kormelink, P.J., Luyten, W.H., Colquhoun, D. & Sivilotti, L.G. (1998) A reporter mutation approach shows incorporation of the 'orphan' subunit beta3 into a functional nicotinic receptor. J. Biol. Chem., 273, 15317-15320.
17. Hallanger, A.E., Levey, A.I., Lee, H.J., Rye, D.B. & Wainer, B.H. (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neurol., 262, 105-124.
18. Hallanger, A.E. & Wainer, B.H. (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J. Comp. Neurol., 274, 483-515.
19. Ikemoto, S., Kohl, R.R. & McBride, W.J. (1997) GABA (A) receptor blockade in the anterior ventral tegmental area increases extracellular levels of dopamine in the nucleus accumbens of rats. J. Neurochem., 69, 137-143.
20. Kelly, P.H. & Iversen, S.D. (1976) Selective 6OHDA-induced destruction of mesolimbic dopamine neurons: abolition of psychostimulant-induced locomotor activity in rats. Eur. J. Pharmacol., 40, 45-56.
21. Klink, R., de Kerchove d'Exaerde, A., Zoli, M. & Changeux, J.P. (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J. Neurosci., 21, 1452-1463.
22. Koob, G.F. (1992) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol. Sci., 13, 177-184.
23. Kuryatov, A., Olale, F., Cooper, J., Choi, C. & Lindstrom, J. (2000) Human alpha6 AChR subtypes: subunit composition, assembly, and pharmacological responses. Neuropharmacology, 39, 2570-2590.
24. Le Novère, N., Zoli, M. & Changeux, J.P. (1996) Neuronal nicotinic receptor alpha 6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur. J. Neurosci., 8, 2428-2439.
25. Lee, H.J., Rye, D.B., Hallanger, A.E., Levey, A.I. & Wainer, B.H. (1988) Cholinergic vs. noncholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J. Comp. Neurol., 275, 469-492.
26. Louis, E.D., Ford, B., Lee, H., Andrews, H. & Cameron, G. (1998) Diagnostic criteria for essential tremor: a population perspective. Arch. Neurol., 55, 823-828.
27. Malagié, I., Trillat, A.C., Douvier, E., Anmella, M.C., Dessalles, M.C., Jacquot, C. & Gardier, A.M. (1996) Regional differences in the effect of the combined treatment of WAY 100635 and fluoxetine: an in vivo microdialysis study. Naunyn-Schmiedeberg's Arch. Pharmacol., 354, 785-790.
28. Mansvelder, H.D. & McGehee, D.S. (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron, 27, 349-357.
29. Marks, M.J., Smith, K.W. & Collins, A.C. (1998) Differential agonist inhibition identifies multiple epibatidine binding sites in mouse brain. J. Pharmacol. Exp. Therap., 285, 377-386.
30. Marubio, L.M., Arroyo-Jimenez, M.M., Cordero-Erausquin, M., Léna, C., Le Novère, N., Huchet, M., Damaj, M.I. & Changeux, J.P. (1999) Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature, 398, 805-810.
31. Nelson, M.E. & Lindstrom, J. (1999) Single channel properties of human alpha3 AChRs: impact of beta2, beta4 and alpha5 subunits. J. Physiol. (Lond.), 516, 657-678.
32. Nicola, S.M. & Deadwyler, S.A. (2000) Firing rate of nucleus accumbens neurons is dopamine-dependent and reflects the timing of cocaine-seeking behavior in rats on a progressive ratio schedule of reinforcement. J. Neurosci., 20, 5526-5537.
33. Oakman, S.A., Fads, P.L., Kerr, P.E., Cozzari, C. & Hartman, B.K. (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci., 15, 5859-5869.
34. Parker, M.J., Beck, A. & Luetje, C.W. (1998) Neuronal nicotinic receptor beta2 and beta4 subunits confer large differences in agonist binding affinity. Mol. Pharmacol., 54, 1132-1139.
35. Picciotto, M.R., Zoli, M., Rimondini, R., Léna, C., Marubio, L.M., Pich, E.M., Fuxe, K. & Changeux, J.P. (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature, 391, 173-177.
36. Pidoplichko, V.I., DeBiasi, M., Williams, J.T. & Dani, J.A. (1997) Nicotine activates and desensitizes midbrain dopamine neurons. Nature, 390, 401-404.
37. Pontieri, F.E., Tanda, G., Orzi, F. & Di Chiara, G. (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature, 382, 255-257.
38. Ramirez-Latorre, J. YuC.R., Qu, X., Perin, F., Karlin, A. & Role, L. (1996) Functional contributions of alpha5 subunit to neuronal acetylcholine receptor channels. Nature, 380, 347-351.
39. Rose, J.E. & Corrigall, W.A. (1997) Nicotine self-administration in animals and humans: similarities and differences. Psychopharmacology (Berl.), 130, 28-40.
40. Ross, S.A., Wong, J.Y., Clifford, J.J., Kinsella, A., Massalas, J.S., Horne, M.K., Scheffer, I.E., Kola, I., Waddington, J.L., Berkovic, S.F. & Drago, J. (2000) Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J. Neurosci., 20, 6431-6441.
41. Sivilotti, L.G., McNeil, D.K., Lewis, T.M., Nassar, M.A., Schoepfer, R. & Colquhoun, D. (1997) Recombinant nicotinic receptors, expressed in Xenopus oocytes, do not resemble native rat sympathetic ganglion receptors in single-channel behaviour. J. Physiol. (Lond.), 500, 123-138.
42. Stolerman, I.P., Bunker, P. & Jarvik, M.E. (1974) Nicotine tolerance in rats; role of dose and dose interval. Psychopharmacologia, 34, 317-324.
43. Stolerman, I.P., Fink, R. & Jarvik, M.E. (1973) Acute and chronic tolerance to nicotine measured by activity in rats. Psychopharmacologia, 30, 329-342.
44. Whiteaker, P., McIntosh, J.M., Luo, S., Collins, A.C. & Marks, M.J. (2000) 125I-alpha-conotoxin MII identifies a novel nicotinic acetylcholine receptor population in mouse brain. Mol. Pharmacol., 57, 913-925.
45. Whiteaker, P., Peterson, C.G., Xu, W., McIntosh, J.M., Paylor, R., Beaudet, A.L., Collins, A.C. & Marks, M.J. (2002) Involvement of the alpha3 subunit in central nicotinic binding populations. J. Neurosci., 22, 2522-2529.
46. Zoli, M., Léna, C., Picciotto, M.R. & Changeux, J.P. (1998) Identification of four classes of brain nicotinic receptors using beta-2 mutant mice. J. Neurosci., 18, 4461-4472.