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The Journal of Neuroscience, November 16, 2005, 25(46):10617-10626; doi:10.1523/JNEUROSCI.2015-05.2005

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Cellular/Molecular
Identification of Molluscan Nicotinic Acetylcholine Receptor (nAChR) Subunits Involved in Formation of Cation- and Anion-Selective nAChRs

Pim van Nierop,¹ Angelo Keramidas,² Sonia Bertrand,² Jan van Minnen,¹ Yvonne Gouwenberg,¹ Daniel Bertrand,² and August B. Smit¹

¹Department of Molecular and Cellular Neurobiology, Center for Neurogenomics and Cognitive Research, Faculty of Earth and Life Sciences, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands, and ²Department of Neuroscience, University Medical Centre, 1211 Geneva 4, Switzerland

Acetylcholine (ACh) is a neurotransmitter commonly found in all animal species. It was shown to mediate fast excitatory and inhibitory neurotransmission in the molluscan CNS. Since early intracellular recordings, it was shown that the receptors mediating these currents belong to the family of neuronal nicotinic acetylcholine receptors and that they can be distinguished on the basis of their pharmacology. We previously identified 12 Lymnaea cDNAs that were predicted to encode ion channel subunits of the family of the neuronal nicotinic acetylcholine receptors. These Lymnaea nAChRs can be subdivided in groups according to the residues supposedly contributing to the selectivity of ion conductance. Functional analysis in Xenopus oocytes revealed that two types of subunits with predicted distinct ion selectivities form homopentameric nicotinic ACh receptor (nAChR) subtypes conducting either cations or anions. Phylogenetic analysis of the nAChR gene sequences suggests that molluscan anionic nAChRs probably evolved from cationic ancestors through amino acid substitutions in the ion channel pore, a mechanism different from acetylcholine-gated channels in other invertebrates.

Key words: Lymnaea stagnalis; cholinergic receptor; ion selectivity; Xenopus oocyte expression; mutation; evolution

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Received May 19, 2005; revised September 29, 2005; accepted October 3, 2005.

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