Arrangement of Cholinoreceptors on the Neuronal Membrane of Two Pulmonate Gastropods

Vulfius, E. A.; Veprintzev, B. N.; Zeimal, E.V.; Michelson, M.J.

doi:10.1038/216400a0

Cited by 18 publications

(9 citation statements)

References 2 publications

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“…From the moment of the identification of ACh as a neurotransmitter, the receptors of ACh have been investigated in the CNS of molluscs by means of electrophysiology (8,9,12,13,32,33). Molluscan CNS studies, as opposed to those in mammalian species, demonstrated that fast AChmediated synaptic transmission is predominant in the CNS and is mediated by multiple and unique nAChR subtypes (10, 11, 34 -36).…”

Section: Discussionmentioning

confidence: 99%

“…In particular, in well described neuronal networks, various nAChR subtypes were shown to mediate synaptic transmission (10,11). Uniquely, molluscs possess excitatory and inhibitory nAChR subtypes conducting cations and anions, respectively (9,(12)(13)(14)(15). Also, different excitatory and inhibitory nAChR subtypes mediate cholinergic transmission at single identified synapses, the differential contribution of which is regulated by soluble extracellular factors (11,16).…”

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confidence: 99%

“…In contrast, in the molluscan CNS, the mode of fast synaptic cholinergic transmission seems to prevail. The CNS of the freshwater snail Lymnaea stagnalis consists of ϳ20,000 large and identifiable neurons, of which many were shown to express functional nicotinic acetylcholine receptors (8,9). In particular, in well described neuronal networks, various nAChR subtypes were shown to mediate synaptic transmission (10,11).…”

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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

Nierop

Bertrand²,

Munno

et al. 2006

Journal of Biological Chemistry

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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 ϳ10% 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. Nicotinic acetylcholine receptors (nAChRs)3 belong to the Cys loop family of pentameric ligand-gated ion channels (LGICs) together with the 5-HT 3 , GABA type A/C, and glycine receptors. nAChRs consist of an extracellular ligand-binding domain (LBD), a transmembrane ion channel, and an intracellular domain (1). In the mammalian central nervous system (CNS), eight ␣-type (␣2-7 and ␣9 -10) and three ␤-type (␤2-4). nAChR subunits have been identified that selectively assemble into nAChR subtypes with different pharmacology, cation conductance, and cellular localization. In the mammalian CNS, nAChRs predominantly mediate presynaptic modulation of neurotransmitter release (for example see Ref.2) and are to a limited extent involved in direct, fast synaptic transmission (for example see Refs. 3-7). In contrast, in the molluscan CNS, the mode of fast synaptic cholinergic transmission seems to prevail. The CNS of the freshwater snail Lymnaea stagnalis consists of ϳ20,000 large and identifiable neurons, of which many were shown to express functional nicotinic acetylcholine receptors (8, 9). In particular, in well described neuronal networks, various nAChR subtypes were shown to mediate synaptic transmission (10, 11). Uniquely, molluscs possess excitatory and inhibitory nAChR subtypes conducting cations and anions, respectively (9, 12-15). Also, different excitatory and inhibitory nAChR subtypes mediate cholinergic transmission at single identified synapses, the differential contribution of which is regulated by soluble extracellular factors (11, 16). Therefore, functio...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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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

Nierop

Bertrand²,

Munno

et al. 2006

Journal of Biological Chemistry

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“…Unlike in the vertebrate nervous system, cholinergic transmission in the molluscan CNS is known to be mediated by cation-and anion-selective nAChRs (Tauc and Gerschenfeld, 1962;Vulfius et al, 1967;Kehoe, 1972aKehoe, ,b, 1976Chemeris et al, 1982). Kehoe and McIntosh (1998) demonstrated the expression of two different anion-selective nAChR subtypes by identified cells in the buccal ganglia of Aplysia.…”

Section: Discussionmentioning

confidence: 99%

“…Molluscan species, however, are long known to display, in addition to excitatory, sodium-selective nAChRs, inhibitory chloride-selective nAChRs, suggesting that a natural recombination event of ligand specificity and ion selectivity has occurred during evolution of molluscan nAChRs (Tauc and Gerschenfeld, 1962;Vulfius et al, 1967Vulfius et al, , 2005Kehoe, 1972aKehoe, ,b, 1976Chemeris et al, 1982). Indeed, recently, acetylcholine-gated anionic channels have been characterized in Caenorhabditis elegans that are overall most similar to mammalian GABARs and GlycRs (Putrenko et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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

Nierop¹,

Keramidas²,

Bertrand³

et al. 2005

J. Neurosci.

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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.

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Amine and Amino Acid Receptors in Gastropod Neurons

Ascher

Kehoe

1975

Amino Acid Neurotransmitters

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Arrangement of Cholinoreceptors on the Neuronal Membrane of Two Pulmonate Gastropods

Cited by 18 publications

References 2 publications

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

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

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

Amine and Amino Acid Receptors in Gastropod Neurons

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