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The Journal of Neuroscience, August 27, 2003, 23(21):7820-7829

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Subunit Composition of Functional Nicotinic Receptors in Dopaminergic Neurons Investigated with Knock-Out Mice

Nicolas Champtiaux,1 Cecilia Gotti,2 Matilde Cordero-Erausquin,1 Denis J. David,3 Cédric Przybylski,3 Clément Léna,1 Francesco Clementi,2 Milena Moretti,2 Francesco M. Rossi,1 Nicolas Le Novère,1 J. Michael McIntosh,4 Alain M. Gardier,3 and Jean-Pierre Changeux1

1Laboratoire de Neurobiologie Moléculaire, Centre National de la Recherche Scientifique Unité de Recherche Associée 2182 "Récepteurs et Cognition," Institut Pasteur, 75724 Paris Cedex 15, France, 2Consiglio Nazionale delle Ricerche, Institute of Neuroscience, Section of Cellular and Molecular Pharmacology, Department of Medical Pharmacology and Center of Excellence on Neurodegenerative Diseases, University of Milan, 20129 Milan, Italy, 3Laboratoire de Neuropharmacologie Equipe Associée-Ministere de l'Education Nationale de la Recherche et de la Technologie, Faculté de Pharmacie Institut Fédératif de Recherche-Institut de Signalisation at Innovation Thérapeutique, Institut de Signalisation et d'Innovation Thérapeutique, Université Paris-Sud, F92296 Châtenay-Malabry cedex, France, and 4Departments of Psychiatry and Biology, University of Utah, Salt Lake City, Utah 84112

Nicotinic acetylcholine receptors (nAChRs) expressed by dopaminergic (DA) neurons have long been considered as potential therapeutic targets for the treatment of several neuropsychiatric diseases, including nicotine and cocaine addiction or Parkinson's disease. However, DA neurons express mRNAs coding for most, if not all, neuronal nAChR subunits, and the subunit composition of functional nAChRs has been difficult to establish. Immunoprecipitation experiments performed on mouse striatal extracts allowed us to identify three main types of heteromeric nAChRs ({alpha}4{beta}2*, {alpha}6{beta}2*, and {alpha}4{alpha}6{beta}2*) in DA terminal fields. The functional relevance of these subtypes was then examined by studying nicotine-induced DA release in striatal synaptosomes and recording ACh-elicited currents in DA neurons from{alpha}4, {alpha}6, {alpha}4{alpha}6, and {beta}2 knock-out mice. Our results establish that {alpha}6{beta}2* nAChRs are functional and sensitive to {alpha}-conotoxin MII inhibition. These receptors are mainly located on DA terminals and consistently do not contribute to DA release induced by systemic nicotine administration, as evidenced by in vivo microdialysis. In contrast, (non{alpha}6){alpha}4{beta}2* nAChRs represent the majority of functional heteromeric nAChRs on DA neuronal soma. Thus, whereas a combination of {alpha}6{beta}2* and {alpha}4{beta}2* nAChRs may mediate the endogenous cholinergic modulation of DA release at the terminal level, somato-dendritic (non{alpha}6){alpha}4{beta}2* nAChRs most likely contribute to nicotine reinforcement.

Key words: dopamine; knock-out mice; mesencephalon; nicotinic acetylcholine receptors; striatum; {alpha}-conotoxine MII

Received March 31, 2003; revised June 24, 2003; accepted July 7, 2003.




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