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J. Biol. Chem., Vol. 281, Issue 3, 1680-1691, January 20, 2006

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Identification and Functional Expression of a Family of Nicotinic Acetylcholine Receptor Subunits in the Central Nervous System of the Mollusc Lymnaea stagnalis^*

Pim van Nierop1, Sonia Bertrand, David W. Munno¶, Yvonne Gouwenberg, Jan van Minnen, J. David Spafford||, Naweed I. Syed¶, Daniel Bertrand, and August B. Smit2

From the Department of Molecular and Cellular Neurobiology, Center for Neurogenomics and Cognition Research, Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1087, 1081 HV Amsterdam, The Netherlands, the Department of Neuroscience, University Medical Centre, 1, rue Midrel Servet, 1211 Geneva 4, Switzerland, the ^¶Department of Cell Biology and Anatomy, University of Calgary, T2N4N1 Calgary, Alberta, Canada, and ^||Cellular and Molecular Neurobiology Research Group, University of Calgary, T2N 4N1 Calgary, Alberta, Canada

We described a family of nicotinic acetylcholine receptor (nAChR) subunits underlying cholinergic transmission in the central nervous system (CNS) of the mollusc Lymnaea stagnalis. By using degenerate PCR cloning, we identified 12 subunits that display a high sequence similarity to nAChR subunits, of which 10 are of the -type, 1 is of the -type, and 1 was not classified because of insufficient sequence information. Heterologous expression of identified subunits confirms their capacity to form functional receptors responding to acetylcholine. The -type subunits can be divided into groups that appear to underlie cation-conducting (excitatory) and anion-conducting (inhibitory) channels involved in synaptic cholinergic transmission. The expression of the Lymnaea nAChR subunits, assessed by real time quantitative PCR and in situ hybridization, indicates that it is localized to neurons and widespread in the CNS, with the number and localization of expressing neurons differing considerably between subunit types. At least 10% of the CNS neurons showed detectable nAChR subunit expression. In addition, cholinergic neurons, as indicated by the expression of the vesicular ACh transporter, comprise 10% of the neurons in all ganglia. Together, our data suggested a prominent role for fast cholinergic transmission in the Lymnaea CNS by using a number of neuronal nAChR subtypes comparable with vertebrate species but with a functional complexity that may be much higher.

Received for publication, August 4, 2005 , and in revised form, November 7, 2005.

^* This work was supported in part by the Swiss National Science Foundation grant (to D. B.) and a Natural Science and Engineering Council of Canada grant (to N. I. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Fig. 5.

¹ Recipient of a grant from the Netherlands Organization for Scientific Research and Technology Foundation Stichting Toegepaste Wetenschappen (STW).

² To whom correspondence should be addressed: Dept. of Molecular and Cellular Neurobiology, Center for Neurogenomics and Cognitive Research, Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands. Tel.: 31-20-5987116; Fax: 31-20-5987112; E-mail: guus.smit{at}falw.vu.nl.

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