Advertisement
Mini review| Volume 97, ISSUE 1, P1-11, April 18, 2002

Nicotinic acetylcholine receptors in autonomic ganglia

      Nicotinic acetylcholine receptors (nAChRs) are the members of a gene superfamily of ionotropic that are formed by five homologous subunits oriented around a central ionic channel. This superfamily includes, in addition to nAChRs, 5-HT3 receptors, GABAA receptors and glycine receptors, but not structurally different glutamate receptors and purinoreceptors (see
      • Lindstrom J.
      Neuronal nicotinic acetylcholine receptors.
      ). The nAChRs are known to mediate fast synaptic transmission in centrifugal and peripheral reflex pathways of all autonomic ganglia and plexuses. Although some recent results suggest this function can also be fulfilled by some other receptors, e.g., P2x purinoreceptors (
      • Evans R.J.
      • Derkach V.A.
      • Surprenant A.
      ATP mediates fast synaptic transmission in mammalian neurons.
      ; see for review
      • Galligan J.J.
      • Bertrand J.P.
      ATP mediates fast synaptic potentials in enteric neurons.
      ), or 5-HT3 (serotonin) receptors (
      • Derkach V.
      • Surprenant A.
      • North R.A.
      5-HT 3 receptors are membrane ion channels.
      ; see for review
      • Khakh B.S.
      • Henderson G.
      Modulation of fast synaptic transmission by presynaptic ligand-gated cation channels.
      ), the evidence for their role in fast transmission in normal (non-cultured) ganglion neurons is still scarce. Although nAChRs are abundantly located in the central nervous system (CNS), most electrophysiological approaches failed to demonstrate their mediatory role in fast synaptic transmission, except in Renshaw cells (see, however,
      • Zaninetti M.
      • Tribollet E.
      • Bertrand D.
      • Raggenbass M.
      Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat.
      ,
      • Marrubio L.M.
      • Arroyo-Jimenez M.D.
      • Cordero-Erausquin M.
      • Lena C.
      • Le Novere N.
      • D Exaerde A.D.
      • Huchet M.
      • Damaj M.I.
      • Changeux J.P.
      Reduced antinociception in mice lacking neuronal nicotinic receptor subunits.
      ). This peculiarity suggests that nAChRs in CNS may be involved in some forms of nonsynaptic neurotransmission (
      • Vidal C.
      • Changeux J.-P.
      Neuronal nicotinic acetylcholine receptors in the brain.
      ). Interestingly, most recent studies showed that, in addition to postsynaptic localization, some nAChRs are localized on terminal buttons, and can cause a significant calcium influx in the buttons, thus modulating the neurotransmitter release (see
      • Itier V.
      • Bertrand D.
      Neuronal nicotinic receptors: from protein structure to function.
      for review).

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Albuquerque E.X.
        • Pereira E.F.
        • Castro N.G.
        • Alkondon M.
        • Reinhardt S.
        • Schroeder H.
        • Maelicke A.
        Nicotinic receptor function in the mammalian nervous system.
        Ann. N. Y. Acad. Sci. 1995; 757: 48-72
        • Albuquerque E.X.
        • Preira E.F.R.
        • Braga M.F.M.
        • Matsubayashi H.
        • Alkondon M.
        Neuronal nicotinic receptors modulate synaptic function in the hippocampus and are sensitive to blockade by the convulsant strychnine and by the anti-Parkinson drug amantadine.
        Toxicol. Lett. 1998; 103: 211-218
        • Alkondon M.
        • Roch E.S.
        • Maelike A.
        • Albuquerque E.X.
        Diversity of nicotinic acetylcholine receptors in the brain: V. Alpha-bungarotoxin-sensitive nicotinic receptors in olfactory bulb neurons and presynaptic modulation of glutamate release.
        J. Pharmacol. Exp. Ther. 1996; 278: 1460-1471
        • Alkondon M.
        • Pereira E.F.R.
        • Cortes W.S.
        • Maelicke A.
        • Albuquerque E.X.
        Choline is a selective agonist of alpha-7 nicotinic acetylcholine receptors in the rat brain neurons.
        Eur. J. Neurosci. 1997; 9: 2734-2742
        • Arias H.R.
        • Blanton M.P.
        Alpha-conotoxins.
        Int. J. Biochem. Cell Biol. 2000; 32: 1017-1028
        • Arroyo-Jimenez M.D.
        • Bourgeois J.P.
        • Marubio L.M.
        • Le Sourd A.M.
        • Ottersen O.P.
        • Rinvik E.
        • Fairen A.
        • Changeux J.P.
        Ultrastructural localization of the alpha-4-subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra.
        J. Neurosci. 1999; 19: 6475-6487
        • Bibevski S.
        • Zhou Y.F.
        • McIntosh J.M.
        • Zigmond R.E.
        • Dunlap M.E.
        Functional nicotinic acetylcholine receptors that mediate ganglionic transmission in cardiac parasympathetic neurons.
        J. Neurosci. 2000; 20: 5076-5082
      1. Bobryshev, A., Skok, V. East excitatory postsynaptic currents in neurons of the rabbit pelvic plexus, in press.

        • Boehm S.
        • Huck S.
        • Freissmuth M.
        Involvement of a phorbol-in-sensitive protein kinase C in the p2-adrenergic inhibition of voltage-gated calcium current in chick sympathetic neurons.
        J. Neurosci. 1996; 16: 4596-4683
        • Boorman J.P.B.
        • Groot-Kormelink P.J.
        • Sivilotti L.G.
        Stoichiometry of human recombinant neuronal nicotinic receptors containing the beta-3 subunit expressed in Xenopus oocytes.
        J. Physiol. 2000; 529: 565-577
        • Briggs C.A.
        • McKenna O.G.
        Effect of MK-801 at the human alpha-7 nicotinic acetylcholine receptor.
        Neuropharmacology. 1996; 35: 407-414
        • Broide R.S.
        • Leslie F.M.
        The alpha-7 nicotinic acetylcholine receptor in neuronal plasticity.
        Mol. Neurobiol. 1999; 20: 1-16
        • Broxton N.
        • Miranda L.
        • Gehrmann J.
        • Down J.
        • Alewood P.
        • Livett B.
        Leu10 of alpha-conotoxin PnIB confers potency for neuronal nicotinic responses in bovine chromaffin cells.
        Eur. J. Pharmacol. 2000; 390: 229-236
        • Brovtsyna N.B.
        • Tikhonov D.B.
        • Gorbunova O.B.
        • Gmiro V.E.
        • Serduk S.E.
        • Lukomskaya N.Y.
        • Magazanik L.G.
        • Zhorov B.S.
        Architecture of the neuronal nicotinic acetylcholine receptor ion channel at the binding site of bis-ammonium blockers.
        J. Membr. Biol. 1996; 152: 77-87
        • Buisson B.
        • Bertrand D.
        Open-channel blockers at the human alpha-4 beta-2 neuronal nicotinic acetylcholine receptor.
        Mol. Pharmacol. 1998; 53: 555-563
        • Cachelin A.B.
        • Rust G.
        Beta-subunits co-determine the sensitivity of rat neuronal nicotinic receptors to antagonists.
        Pfluegers Arch.-Eur. J. Physiol. 1995; 429: 449-451
        • Cassel J.F.
        • Clark A.L.
        • McLachlan E.M.
        Characteristics of fasic and ionic sympathetic ganglia cells of the guinea-pig.
        J. Physiol. 1986; 372: 457-483
        • Chang K.T.
        • Berg D.K.
        Nicotinic acetylcholine receptors containing alpha-7subunits are required for reliable synaptic transmission in situ.
        J. Neurosci. 1999; 19: 3701-3710
        • Chavez-Noriega L.E.
        • Gillespie A.
        • Stauderman K.A.
        • Crona J.H.
        • Claeps B.D.
        • Elliott K.J.
        • Reid R.T.
        • Rao T.S.
        • Velicelebi G.
        • Harpold M.M.
        • Johnson E.C.
        • Corey-Naeve J.
        Characterization of the recombinant human neuronal nicotinic acetylcholine receptors alpha-3 beta-2 and alpha-4 beta-2 stably expressed in HEK293 cells.
        Neuropharmacology. 2000; 39: 2543-2560
        • Colquhoun D.
        • Hawkes A.G.
        The principles of the stochastic interpretation of ion-channel mechanisms.
        in: Sakmann B. Neher E. Single-Channel Recording. Plenum, New York1983: 135-175
        • Colquhoun L.M.
        • Patrick J.W.
        Alpha-3, beta-2, and beta-4 form heterotrimeric neuronal nicotinic acetylcholine receptos in Xenopus oocytes.
        J. Neurochem. 1997; 69: 2355-2362
        • Colquhoun L.M.
        • Patrick J.W.
        Pharmacology of neuronal nicotinic acetylcholine receptor subtypes.
        Adv. Pharmacol. 1997; 39: 191-220
        • Conti-Fine B.M.
        • Maelicke A.
        • Reinhardt-Maekicke S.
        • Chiappinelli V.
        • Mclane K.E.
        Binding sites for neurotoxins and clolinergic ligands in peripheral and neuronal nicotinic receptors.
        Ann. N. Y. Acad. Sci. 1995; 757: 133-152
        • Conroy W.
        • Berg D.
        Neurons can maintain multiple classes of nicotinic acetycholine receptors distinguished by different subunit compositions.
        J. Biol. Chem. 1995; 270: 4424-4431
        • Corringer P.-J.
        • Bertrand S.
        • Galzi J.-L.
        • Devillers-Thiery A.
        • Changeux J.-P.
        • Bertrand D.
        Mutational analysis of the charge selectivity filter of the alpha-7 nicotinic acetylcholine receptor.
        Neuron. 1999; 22: 831-843
        • Corriveau R.
        • Berg D.
        Coexpression of multiple acetylcholine receptor genes in neurons. Quantification of transcripts during development.
        J. Neurosci. 1993; 13: 2662-2671
        • Covernton P.
        • Kojima H.
        • Sivilotti L.
        • Gibb A.
        • Colquhoun D.
        Comparison of neuronal nicotinic receptors in rat sympathetic neurons with subunit pairs expressed in Xenopus oocytes.
        J. Physiol. 1994; 481: 27-34
        • Cuevas J.
        • Adams D.J.
        Local anaesthetic blockade of neuronal nicotinic ACh receptor-channels in rat parasympathetic ganglion cells.
        Br. J. Pharmacol. 1994; 111: 663-672
        • Cuevas J.
        • Berg D.K.
        Mammalian nicotinic receptors with alpha-7 subunits that slowly desensitize and rapidly recover from alpha-bungarotoxin blockade.
        J. Neurosci. 1998; 18: 10335-10344
        • D'Amour K.A.
        • Casida J.E.
        Desnitroimidaclorid and nicotine binding site in rat recombinant alpha-4 beta-2 neuronal nicotinic catylcholine receptor.
        Pestic. Biochem. Physiol. 1999; 64: 55-61
        • Dani J.A.
        • Elsenman G.
        Monovalent and divalent cation permeation in acetylcholine receptor channels.
        J. Gen. Physiol. 1987; 89: 959-983
        • Davies A.R.L.
        • Hardick D.J.
        • Blagbrough I.S.
        • Potter B.V.L.
        • Wolstenholm A.J.
        • Wonnacott S.
        Characterisation of the binding of [3H] methyllycaconitine: a new radioligand for labelling alpha7-type neuronal nicotinic acetylcholine receptors.
        Neuropharmacology. 1999; 38: 679-690
        • Derkach V.A.
        • Selyanko A.A.
        • Skok V.I.
        Acetylcholine-induced current fluctuations and fast excitatory postsynaptic currents in rabbit sympathetic neurons.
        J. Physiol. 1983; 336: 511-526
        • Derkach V.A.
        • North R.A.
        • Selyanko A.A.
        • Skok V.I.
        Single channels activated by acetylcholine in rat superior cervical ganglion.
        J. Physiol. 1987; 388: 141-151
        • Derkach V.
        • Surprenant A.
        • North R.A.
        5-HT 3 receptors are membrane ion channels.
        Nature. 1989; 339: 706-709
        • Derkach V.A.
        • Kurenny D.E.
        • Melishchuk A.I.
        • Selyanko A.A.
        • Skok V.I.
        Role of disulfide bonds in burst-like activity of nicotinic acetylcholine receptor channels in rat sympathetic neurones.
        J. Physiol. (London). 1991; 440: 1-15
        • Drisdel R.C.
        • Green W.N.
        Neuronal alpha-bungarotoxin receptors are alpha-7 subunit homomers.
        J. Neurosci. 2000; 20: 133-139
        • Evans R.J.
        • Derkach V.A.
        • Surprenant A.
        ATP mediates fast synaptic transmission in mammalian neurons.
        Nature. 1992; 357: 503-506
        • Ferreira M.
        • Ebert S.N.
        • Perry D.C.
        • Yasuda R.P.
        • Baker C.M.
        • Davila-Garcia M.I.
        • Kellar K.J.
        • Gillis R.A.
        Evidence of a functional alpha7-neuronal nicotinic receptor subtype located on motoneurons of the dorsal motor nucleus of the vagus.
        J. Pharmacol. Exp. Ther. 2001; 296: 260-269
        • Figl A.
        • Cohen B.N.
        The beta subunit dominates the relaxation kinetics of heteromeric neuronal nicotinic receptors.
        J. Physiol. 2000; 524: 685-699
        • Figl A.
        • Cohen B.N.
        • Quick M.W.
        • Yang X.C.
        • Lester H.A.
        Regions of beta-4, beta-2 subunit chimera that contribute to the agonist selectivity of neuronal nicotinic receptors.
        FEBS Lett. 1992; 308: 245-248
        • Flora A.
        • Schulz R.
        • Benfante R.
        • Battaglioli E.
        • Terzano S.
        • Clementi F.
        • Fornasari D.
        Neuronal and extraneuronal expression and requlation of the human alpha-5 nicotinic receptor subunit gene.
        J. Neurochem. 2000; 75: 18-27
        • Francis M.M.
        • Vazquez R.W.
        • Papke R.L.
        • Oswald R.E.
        Subtype-selective inhibition of neuronal nicotinic acetylcholine receptors by cocaine is determined by the alpha-4 and beta-4 subunits.
        Mol. Pharmacol. 2000; 58: 109-119
        • Fucile S.
        • Palma E.
        • Mileo A.M.
        • Miledi R.
        • Eusebi F.
        Human neuronal threonine-for-leucine-248 alpha-7 mutant nicotinic acetylcholine receptors are highly Ca2+ permeable.
        Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 3643-3648
        • Galligan J.J.
        • Bertrand J.P.
        ATP mediates fast synaptic potentials in enteric neurons.
        J. Neurosci. 1994; 14: 7563-7571
        • Galligan J.J.
        • North R.A.
        MK-801 blocks nicotinic depolarizations of guinea pig myenteric neurones.
        Neurosci. Lett. 1990; 108: 105-109
        • Galzi J.-L.
        • Changeux J.-P.
        Neurotransmitter-gated ion channels as unconventional allosteric proteins.
        Curr. Opin. Struct. Biol. 1994; 4: 554-565
        • Galzi J.-L.
        • Changeux J.-P.
        Neuronal nicotinic receptors molecular organization and regulations.
        Neuropharmacology. 1995; 34: 563-582
        • Galzi J.L.
        • Revah F.
        • Black D.
        • Goeldner M.
        • Hirth C.
        • Changeux J.P.
        Identification of a novel amino acid a tyrosine 93 within the cholinergic ligand-binding sites of the acetylcholine receptor by photoaffinity labeling.
        J. Biol. Chem. 1990; 265: 10430-10437
        • Galzi J.L.
        • Bertrand D.
        • Devillers-Thiery A.
        • Revah F.
        • Bertrand S.
        • Changeux J.P.
        Functional significance of aromatic amino acids from three peptide loops of the alpha-7 neuronal nicotinic receptor site investigated by site directed mutagenesis.
        FEBS Lett. 1991; 294: 198-202
        • Galzi J.L.
        • Bertrand S.
        • Corringer P.J.
        • Changeux J.P.
        • Bertrand D.
        Identification of calcium binding sites that regulate potentiation of a neuronal nicotinic acetylcholine receptor.
        EMBO J. 1996; 15 (Oxford Univ. Press): 5824-5832
        • Garcia-Guzman M.
        • Sala F.
        • Sala S.
        • Campos-Caro A.
        • Stuhmer W.
        • Guuttierrez L.M.
        • Criado M.
        Alpha-bungarotoxin-sensitive nicotinic receptors on bovine chromaffin cells: molecular cloning, functional expression and alternative splicing of the alpha 7 subunit.
        Eur. J. Neurosci. 1995; 7: 647-655
        • Gerzanich V.
        • Wang F.
        • Kuryatov A.
        • Lindstrom J.
        Alpha-5 subunit alters desensitization, pharmacology, Ca++ permeability and Ca++ modulation of human neuronal alpha-3 nicotinic receptors.
        J. Pharmacol. Exp. Ther. 1998; 286: 311-320
        • Glushakov A.V.
        • Melishchuk A.I.
        • Skok V.I.
        ATP-induced currents in submucous plexus neurons of the guinea pig small intestine.
        Neurophysiology. 1996; 28: 77-85
        • Glushakov A.V.
        • Glushakova H.Y.
        • Skok V.I.
        Modulation of nicotinic acetylcholine receptor activity in submucous neurons by intracellular messengers.
        JANS. 1999; 75: 16-22
      2. Glushakov, A.V., Voitenko, L.P., Skok, M.V., Skok, V.I. Distribution of neuronal nicotinic acetylcholine receptors containing different alpha-subunits in the submucosal nerve plexus of the quinea-pig, in press.

        • Gotti C.
        • Carbonnelle E.
        • Moretti M.
        • Zwart R.
        • Clementi F.
        Drugs selectiva for nicotinic receptor subtypes: a real possibility or a dream?.
        Behav. Brain Res. 2000; 113: 183-192
        • Hernandez S.C.
        • Bertolino M.
        • Xiao Y.X.
        • Pringle K.E.
        • Caruso F.S.
        • Kellar K.J.
        Dextromethorphan and its metabolite dextrorphan block alpha-3 beta-4 neuronal nicotinic receptors.
        J. Pharmacol. Exp. Ther. 2000; 293: 962-967
        • Herrero C.J.
        • Garcia-Palomero T.
        • Pintado A.J.
        • Garcia A.S.
        • Montiel C.
        Differential blockade of rat alpha-3 beta-4 and alpha-7 neuronal nicotinic receptors by omega-conotoxin MVIIC, omega-conotoxin GVIA and diltiazem.
        Br. J. Pharmacol. 1999; 127: 1375-1387
        • Hogg R.C.
        • Miranda L.P.
        • Craik D.J.
        • Lewis R.J.
        • Alewood P.F.
        • Adams D.J.
        Single amino acid substitutions in alpha-conotoxin PnIA shift selectivity for subtypes of the mammalian neuronal nicotinic acetylcholine receptor.
        J. Biol. Chem. 1999; 274: 36559-36564
        • Horch H.L.
        • Sargent P.B.
        Perisynaptic surface distribution of multiple classes of nicotinic acetylcholine receptors on neurons in the chicken ciliary ganglion.
        J. Neurosci. 1995; 15: 7778-7795
        • Inokuchi H.
        • McLachlan E.M.
        Lack of evidence for P2X-purinoceptor involvement in fast synaptic responses in intact sympathetic ganglia isolated from guinea-pigs.
        Neuroscience. 1995; 69: 651-659
        • Itier V.
        • Bertrand D.
        Neuronal nicotinic receptors: from protein structure to function.
        FEBS Lett. 2001; 504: 118-125
        • Kertser S.
        • Bobryshev A.
        • Voitenko S.
        • Gmiro V.
        • Brovtsyna N.
        • Skok V.
        Dimensions of neuronal nicotinic acetylcholine receptor channel as estimated from the analysis of the channel-blocking effects.
        J. Membr. Biol. 1998; 163: 111-118
        • Khakh B.S.
        • Henderson G.
        Modulation of fast synaptic transmission by presynaptic ligand-gated cation channels.
        JANS. 2000; 81: 110-121
        • Kilmer S.L.
        • Carlsen R.C.
        Forskolin activation of adenylate cyclase in vitro stimulates nerve generation.
        Nature. 1984; 307: 455-456
        • Kurenny D.E.
        • Selyanko A.A.
        • Derkach V.A.
        • Gmiro V.E.
        • Skok V.I.
        Mechanism of long-lasting block of ganglion nicotinic receptors by mono-ammonium compounds with long aliphatic chain.
        JANS. 1994; 48: 231-240
        • Lamthanh H.
        • Jegou-Matheron C.
        • Servent D.
        • Menez A.
        • Lancelin J.M.
        Minimal conformation of the alpha-conotoxin ImI for the alpha-7 neuronal nicotinic acetylcholine receptor recognition: correlated CD, NMR and binding studies.
        FEBS Lett. 1999; 454: 293-298
        • Laurenza A.
        • Sutkowski E.McH.
        • Seamon K.B.
        Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action?.
        Trends Pharmacol. Sci. 1989; 10: 442-447
        • Levandoski M.M.
        • Lin Y.X.
        • Moise L.
        • McLaughlin J.T.
        • Cooper E.
        • Hawrot E.
        Chimeric analysis of a neuronal nicotinic acetylcholine receptor reveals amino acids conferring sensitivity to alpha-bungarotoxin.
        J. Biol. Chem. 1999; 274: 26113-26119
        • Lewis T.M.
        • Harkness P.C.
        • Sivilotti L.G.
        • Colquhoun D.
        • Millar N.S.
        The ion channel properties of a rat recombinant neuronal nicotinic receptor are dependent on the host cell type.
        J. Physiol. 1997; 505: 299-306
        • Lindstrom J.
        Neuronal nicotinic acetylcholine receptors.
        in: Narahashi T. Ion Channels. vol. 4. Plenum, New York1996: 377-390
        • Lindstrom J.
        • Anand R.
        • Reng X.
        • Gerzanich V.
        • Wang F.
        • Li Y.
        Neuronal nicotinic receptor subtypes.
        Ann. N. Y. Acad. Sci. 1995; 757: 100-116
        • Liu O.
        • Melnikova I.N.
        • Hu M.J.
        • Gardner P.D.
        Cell type-specific activation of neuronal nicotinic acetylcholine receptor subunit genes by Sox10.
        J. Neurosci. 1999; 19: 9747-9755
        • Luetje C.
        • Patrick J.
        Both alpha and beta subunits contribute to the sensitivity of neuronal nicotinic acetylcholine receptors.
        J. Neurosci. 1991; 11: 837-845
        • Lukas R.
        • Norman S.
        • Lucero L.
        Characterization of nicotinic acetylcholine receptors expressed by cells of the SH-SY5Y human neuroblastoma clonal line.
        Mol. Cell. Neurosci. 1993; 4: 1-12
        • Mandelzys A.
        • Pie B.
        • Deneris E.
        • Cooper E.
        The developmental increase in acetylcholine current densities on rat sympathetic neurons correlates with changes in nicotinic acetylcholine receptor alpha subunit gene expression and occurs independent on innervation.
        J. Neurosci. 1994; 14: 2357-2364
        • Marrubio L.M.
        • Arroyo-Jimenez M.D.
        • Cordero-Erausquin M.
        • Lena C.
        • Le Novere N.
        • D Exaerde A.D.
        • Huchet M.
        • Damaj M.I.
        • Changeux J.P.
        Reduced antinociception in mice lacking neuronal nicotinic receptor subunits.
        Nature. 1999; 398: 805-810
        • McGehee D.S.
        Molecular diversity of neuronal nicotinic acetylcholine receptors.
        Ann. N. Y. Acad. Sci. 1999; 868: 565-577
        • McIntosh J.M.
        • Santos A.D.
        • Olivera B.M.
        Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes.
        Annu. Rev. Biochem. 1999; 68: 59-88
        • McIntosh J.M.
        • Gardner S.
        • Luo S.Q.
        • Garrett J.E.
        • Yoshikami D.
        Conus peptides: novel probes for nicotinic acetylcholine receptor structure and function.
        Eur. J. Pharmacol. 2000; 393: 205-208
        • Nakasava K.
        ATP-activated current and its interaction with acetylcholine-activated current in rat sympathetic neurons.
        J. Neurosci. 1994; 14: 740-749
        • Nelson M.E.
        • Lindstrom J.L.
        Single channel properties of human alpha3 AchRs: impact of beta2, beta4 and alpha5 subunits.
        J. Physiol. 1999; 516: 657-678
        • Nutter T.J.
        • Adams D.J.
        Monovalent and divalent cation permeability and block of neuronal nicotinic receptor.
        J. Gen. Physiol. 1995; 105: 701-723
        • O'Leary M.E.
        • White M.M.
        Mutational analysis of ligand-induced activation of the torpedo acetylcholine receptor.
        J. Biol. Chem. 1992; 267: 8360-8365
        • Orr-Urtreger A.
        • Goeldner F.M.
        • Saeki M.
        • Lorenzo I.
        • Goldberg L.
        • De Biasi M.
        • Dani J.A.
        • Patrick J.W.
        • Beaudet A.L.
        Mice deficient in the alpha-7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fact nicotinic currents.
        J. Neurosci. 1997; 17: 9165-9171
        • Palma E.
        • Bertrand S.
        • Binzoni T.
        • Bertrand D.
        Neuronal nicotinic alpha-7 receptor expressed in Xenopus oocytes presents five putative binding sites for methyllycaconotine.
        J. Physiol. 1996; 491: 151-161
        • Palma E.
        • Fucile B.
        • Barabino B.
        • Miledi R.
        • Eusebi F.
        Strychnine activates neuronal alpha-7 nicotinic receptors after mutations.
        Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 13421-13426
        • Palmer J.M.
        • Wood J.D.
        • Zafirov D.H.
        Elevation of 3′, 5′-phosphate mimics slow synaptic excitation in myenteric neurones of the guinea-pig.
        J. Physiol. 1986; 376: 451-460
        • Papke R.L.
        • Heinemann S.F.
        The role of the beta-4 subunit in determining the kinetic properties of rat neuronal nicotinic cetylcholine alpha-3 receptors.
        J. Physiol. 1991; 440: 95-112
        • Parker M.J.
        • Beck A.
        • Luitje C.W.
        Neuronal nicotinic receptor beta-2 and beta-4 subunits confer large differences in agonist binding affinity.
        Mol. Pharmacol. 1998; 54: 1132-1139
        • Paterson D.
        • Nordberg A.
        Neuronal nicotinic receptors in the human brain.
        Prog. Neurobiol. 2000; 61: 75-111
        • Rang H.
        The characteristics of synaptic currents and responses to acetylcholine in rat submandibular ganglion cells.
        Br. J. Pharmacol. 1981; 75: 151-158
        • Remizov I.N.
        • Maslov V.Yu.
        • Purnyn E.E.
        • Gmiro V.E.
        • Skok V.I.
        Selective pharmacological blockade of synaptic transmission in parasympathetic pathways to the heart in rats.
        Neurophysiology. 1995; 27: 323-330
        • Rogers M.
        • Colquhoun L.M.
        • Patrick J.W.
        • Dani J.A.
        Calcium flux through predominantly independent purinergic ATP and nicotinic acetylcholine receptors.
        J. Neurophysiol. 1997; 77: 1407-1417
        • Role L.W.
        Diversity, in primary structure and function of neuronal nicotinic acetylcholine receptor channels.
        Curr. Opin. Neurobiol. 1992; 2: 254-262
        • Roth A.L.
        • Shoop R.D.
        • Berg D.K.
        Targeting alpha-7 containing nicotinic receptors on neurons to distal locations.
        Eur. J. Pharmacol. 2000; 393: 105-112
        • Rust G.
        • Burgunder J.-M.
        • Lauterburg T.E.
        • Cachelin A.B.
        Expression of neuronal nicotinic acetylcholine receptor subunit genes in the rat autonomic nervous system.
        Eur. J. Neurosci. 1994; 6: 478-485
        • Rovira J.C.
        • Vicente-Agullo F.
        • Campos-Caro A.
        • Criado M.
        • Sala F.
        • Sala S.
        • Ballesta J.J.
        Gating of alpha-3 beta-4 neuronal nicotinic receptor can be controlled by the loop M2-M3 of both alpha-3 and beta-4 subunits.
        Pfluegers Arch. Eur. J. Physiol. 1999; 439: 86-92
        • Sargent P.B.
        The diversity of neuronal nicotinic acetylcholine receptors.
        Annu. Rev. Neurosci. 1993; 16: 403-443
        • Selyanko A.A.
        • Skok V.I.
        Acetylcholine receptors in rat cardiac neurones.
        JANS. 1992; 40: 33-48
        • Selyanko A.A.
        • Skok V.I.
        Synaptic transmission in rat cardiac neurones.
        JANS. 1992; 39: 191-200
        • Shao Z.Y.
        • Yakel J.L.
        Single channel properties of neuronal nicotinic Ach receptors in stratum radiatum interneurons of rat hippocampal slices.
        J. Physiol. 2000; 527: 507-513
        • Shoop R.D.
        • Martone M.E.
        • Yamada N.
        • Ellisman M.H.
        • Berg D.K.
        Neuronal acetylcholine receptors with alpha-7 subunits are concentrated on somatic spines for synaptic signaling in embryonic chich ciliary ganglia.
        J. Neurosci. 1999; 19: 692-704
        • Shoop R.D.
        • Yamada N.
        • Berg D.K.
        Cytoskeletal links of neuronal acetylcholine receptors containing alpha-7 subunits.
        J. Neurosci. 2000; 20: 4021-4029
        • Skok V.I.
        • Selyanko A.A.
        • Derkach V.A.
        Neuronal Acetylcholine Receptors. Plenum, New York1989 (319 pp.)
        • Skok V.I.
        • Groisman S.D.
        • Melnichenko L.V.
        • Gersanich V.V.
        • Gmiro V.E.
        Selective pharmacological blockade of parasympathetic and enteric ganglia.
        JANS. 1991; 35: 211-218
        • Skok V.I.
        • Voitenko S.V.
        • Kurenniy D.E.
        • Brovtsyna N.B.
        • Gmiro V.E.
        • Kertser S.L.
        The ionic channel of neural nicotinic acetylcholine receptors is funnel-shaped.
        Neuroscience. 1995; 67: 933-939
        • Skok V.I.
        • Farrugia G.
        • Ermilov L.G.
        • Miller S.M.
        • Szurszewski J.H.
        Patch-clamp recordings of membrane currents evoked during natural synaptic activity in sympathetic neurons.
        Neuroscience. 1998; 87: 509-517
        • Skok M.V.
        • Voitenko L.P.
        • Voitenko S.V.
        • Lykhmus E.Y.
        • Kalashnok E.N.
        • Litvin T.I.
        • Tzartos S.J.
        • Skok V.I.
        Alpha subunit composition of nicotinic acetylcholine receptors in the rat autonomic ganglia neurons as determined with subunit-specific anti-alpha(181–192) peptide antibodies.
        Neuroscience. 1999; 93: 427-1436
        • Temburni M.K.
        • Blitzblau R.C.
        • Jacob M.H.
        Receptor targeting and heterogeneity at interneuronal nicotinic cholinergic synapses in vivo.
        J. Physiol. 2000; 525: 21-29
        • Ullian E.M.
        • Mcintosh J.M.
        • Surgent P.B.
        Rapid synaptic transmission in the avian ciliary ganglion is mediated by two distinet classes of nicotinic receptors.
        J. Neurosci. 1997; 17: 7210-7219
        • Unwin N.
        Acetylcholine receptor channel imaged in the open state.
        Nature. 1995; 373: 37-43
        • Vanner S.
        • Surprenant A.
        Effects of 5-HT, receptor antagonists on 5-HT and nicotinic depolarizations in guinea-pig submucosal neurones.
        Br. J. Pharmacol. 1990; 99: 840-844
        • Voitenko S.V.
        • Bobrishev A.U.
        • Skok V.I.
        Effect of tetraethylammonium on nicotinic acetylcholine receptors in rat sympathetic ganglion neurones.
        Mol. Neuropharmacol. 1993; 3: 153-160
        • Voitenko S.V.
        • Gmiro V.E.
        • Artemenko M.I.
        • Skok V.I.
        Blocking of neuronal nicotinic acetylcholine receptors with d-sparteine derivatives.
        Neurophysiology. 1994; 26: 221-224
        • Voitenko L.P.
        • Voitenko S.V.
        • Skok M.V.
        • Purnyn H.E.
        • Skok V.I.
        Nicotinic acetulcholine receptor subtypes in rat superior cervical ganglion neurons as studied by seguential application of two alpha-subunit-specific antibodies.
        Neurosci. Lett. 2001; 303: 37-40
        • Vernalis A.B.
        • Conroy W.G.
        • Berg D.K.
        Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes.
        Neuron. 1993; 10: 451-464
        • Vidal C.
        • Changeux J.-P.
        Neuronal nicotinic acetylcholine receptors in the brain.
        News Physiol. Sci. 1996; 11: 202-208
        • Wang F.
        • Gerzanich V.
        • Wells G.
        • Anand R.
        • Peng X.
        • Keyser K.
        • Lindstrom J.
        Assembly of human neuronal nicotinic receptor alpha-5 subunit with alpha-3, beta-4 subunits.
        J. Biol. Chem. 1996; 271: 17.656-17.665
        • Wecker L.
        • Guo X.
        • Rycerz A.M.
        • Edwards S.C.
        Cyclic AMP-dependent protein kinase (PKA) and protein kinase C prosporylate sites in the amino acid sequence corresponding to the M3/M4 cytoplasmic domain of alpha-4 neuronal nicotinic receptor subunits.
        J. Neurochem. 2001; 76: 711-720
        • Wonnacott S.
        • Albuquerque E.
        • Bertrand D.
        Methyllycaconitine : a new probe that discriminates between nicotinic receptor subciasses.
        Methods Neurosci. 1993; 12: 263-275
        • Wood J.D.
        Electrical and synaptic behavior of enteric neurones.
        in: Wood G.D. Handbook of Physiology. The Gastrointestinal System Motility and Circulation. American Physiological Society, Bethesda, MD, USA1989: 465-517
        • Xiao Y.X.
        • Meyer E.L.
        • Thompson J.M.
        • Surin A.
        • Wroblewski J.
        • Kellar K.J.
        Rat alpha3/beta4 subtype of neuronal nicotinic acetylcholine receptor stably expressed in a transfected cell line: pharmacology of ligand binding and function.
        Mol. Pharmacol. 1998; 54: 322-333
        • Xu W.
        • Orr-Urtreger A.
        • Nigro F.
        • Selber S.
        • Sutcliffe C.B.
        • Armstrong D.
        • Patrick J.W.
        • Role L.W.
        • Beaudet A.L.
        • De Biasi M.
        Multiorgan autonomic dysfunction in mice lacking the beta-2 and the beta-4 subunits of neuronal nicotinic acetylcholine receptors.
        J. Neurosci. 1999; 19: 9298-9305
        • Yawo H.
        Rectification of synaptic and acetylcholine currents in mouse submandibular ganglion cells.
        J. Physiol. 1989; 417: 307-322
      3. Yeh, J.J., Ferreira, M., Ebert, S., Yasuda, R.P., Kellar, Y.J., Wolfe, B.B. Axtomomy and nerve growth factor regulate levels of neuronal nicotinic acetylcholine receptor alpha-3 subunit proteins in rat superior cervical ganglion, in press.

        • Yu C.R.
        • Role L.W.
        Functional contribution of the alpha-7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones.
        J. Physiol. 1998; 509: 651-665
        • Zaninetti M.
        • Tribollet E.
        • Bertrand D.
        • Raggenbass M.
        Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat.
        Eur. J. Neurosci. 1999; 11: 2737-2748
        • Zhang J.
        • Xiao Y.
        • Abdrakhmanova B.
        • Wang W.
        • Cleemann L.
        • Kellar K.J.
        • Morad M.
        Activation and Ca2+ permeation of stablytransfected alpha 3/beta 4 neuronal nicotinic acetylcholine receptor.
        Mol. Pharmacol. 1999; 55: 970-981
        • Zhorov B.S.
        • Brovtsyna N.B.
        • Gmiro V.E.
        • Lukomskya N.Ya.
        • Serdyuk S.E.
        • Potapyeva N.N.
        • Magazanik L.G.
        • Kurenniy D.E.
        • Skok V.I.
        Dimensions of the ion channel in neuronal nicotinic receptor as estimated from analysis of conformation-activity relationships of open-channel blocking drugs.
        J. Membr. Biol. 1991; 121: 119-132