Abstract
The discovery that mammalian brain expresses the mRNAs for nine different nicotinic cholinergic receptor subunits (α2–α7, β2–β4) that form functional receptors when expressed in Xenopus laevis oocytes suggests that many different types of nicotinic cholinergic receptors (nAChRs) might be expressed in the mammalian brain., Using an historical approach, this chapter reviews some of the progress made in identifying the nAChR subtypes that seem to play a vital role in modulating dopaminergic function. nAChR subtypes that are expressed in dopamine neurons, as well as neurons that interact with dopamine neurons (glutamatergic, GABAergic), serve as the focus of this review. Subjects that are highlighted include the discovery of a low affinity α4β2* nAChR, the identity of recently characterized α6* nAChRs, and the finding that these α6* receptors have the highest affinity for receptor activation of any of the native receptors that have been characterized to date. Topics that have been ignored in other recent reviews of this area, such as the discovery and potential importance of alternative transcripts, are presented along with a discussion of their potential importance.
Access provided by Autonomous University of Puebla. Download to read the full chapter text
Chapter PDF
Similar content being viewed by others
Keywords
- Nicotinic Receptor
- Nicotinic Acetylcholine Receptor
- nAChR Subunit
- nAChR Subtype
- Neuronal Nicotinic Acetylcholine Receptor
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
References
Alkondon M, Pereira EFR, Eisenberg HM, Albuquerque EX (1999) Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J Neurosci 19:2693–2705
Anand R, Peng X, Ballesta JJ, Lindstrom J (1993) Pharmacological characterization of α-bungarotoxin-sensitive acetylcholine receptors immunoisolated from chick retina: Contrasting preoperties of α7 and α8 subunit-containing subtypes. Mol Pharmacol 44:1046–1050
Azam L, Winzer-Serhan UH, Chen Y, Leslie FM (2002) Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 444: 260–274
Badio B, Daly JW (1994) Epibatidine, a potent analgetic and nicotinic agonist. Mol Pharmacol 45:563–569
Ballivet M, Nef P, Couturier S, Rungger D, Bader CR, Bertrand D, Cooper E (1988) Electrophysiology of a chick neuronal nicotinic acetylcholine receptor expressed in Xenopus oocytes after cDNA injection. Neuron 1:847–852
Barlow RB, Ing HR (1948) Curare-like action of polymethylene bis-quaternary ammonium salts. Br J Pharma Chemother 3:298–304
Bernard C (1856) Analyse physiologique des propriétés des systèmes musculaires et nerveux au moyen de curare. Comptes rendus hebdomadaires de l'Académie des sciences 43:825–829
Bertrand D, Elmslie F, Hughes E, Trounce J, Sander T, Bertrand S, Steinlein OK (2005) The CHRNB2 mutation I312M is associated with epilepsy and distinct memory deficits. Neurobiol Dis 20:799–804
Bhat RV, Marks MJ, Collins AC (1994) Effects of chronic nicotine infusion on kinetics of highaffinity nicotine binding. J Neurochem 62:574–581
Boulter J, Evans K, Goldman D, Martin G, Treco D, Heinemann S, Patrick J (1986) Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor α-subunit. Nature 319:368–374
Brown RWB, Collins AC, Lindstrom J, Whiteaker P (2007) Nicotinic α5 subunit deletion locally reduces high-affinity agonist activation without altering receptor numbers. J Neurochem 103:204–215
Buisson B, Bertrand D (2001) Chronic exposure to nicotine upregulates the human (alpha)4((beta)2 nicotinic acetylcholine receptor function. J Neurosci 21:1819–1829.
Cartier GE, Yoshikami D, Gray WR, Luo S, Olivera BM, McIntosh JM (1996) A new alphaconotoxin which targets alpha3beta2 nicotinic acetylcholine receptors. J Biol Chem 271: 7522–7528
Champtiaux N, Han ZY, Bessis A, Rossi FM, Zoli M, Marubio L, McIntosh JM, Changeux JP (2002) Distribution and pharmacology of alpha 6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 22:1208–1217
Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knockout mice. J Neurosci 23:7820–7829
Chang CC, Lee CY (1963) Isolation of neurotoxins from the venom of Bungarus multicinctus and their modes of neuromuscular blocking action. Arch Int Pharmacodyn 144:241–257
Changeux J-P, Kasai M, Lee CY (1970) Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci 67:1241–1247
Chavez-Noriega LE, Crona JH, Washburn MS, Elliott KJ, Johnson EC (1997) Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in Xenopus oocytes. J Pharmacol Exp Ther 280:346–356
Chen DN, Patrick JW (1997) The α-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the α7 subunit. J Biol Chem 272:24024–24029
Clarke PBS, Schwartz RD, Paul SM, Pert CB, Pert A (1985) Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-alpha-bungarotoxin. J Neurosci 5:1307–1315
Combi R, Dalpra L, Tenchini ML, Ferini-Strambi L (2004) Autosomal dominant nocturnal frontal lobe epilepsy: A critical overview. J Neurol 251:923–934
Connolly J, Boulter J, Heinemann SF (1992) Alpha 4–2 beta 2 and other nicotinic acetylcholine receptor subtypes as targets of psychoactive and addictive drugs. Br J Pharmacol 105:657–666
Conti-Tronconi BM, Dunn SM, Barnard EA, Dolly JO, Lai FA, Ray N, Raftery MA (1985) Brain and muscle nicotinic acetylcholine receptors are different but homologous proteins. Proc Natl Acad Sci U S A 82:5208–5212
Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5:847–856
Cuevas J, Berg DK (1998) Mammalian nicotinic receptors with α7 subunits that slowly desensitize and rapidly recover from α-bungarotoxin blockade. J Neurosci 18:10335–10344
Cui C, Booker TK, Allen RS, Grady SR, Whiteaker P, Marks MJ, Salminen O, Tritto T, Butt CM, Allen WR, Stitzel JA, McIntosh JM, Boulter J, Collins AC, Heinemann SF (2003) The beta3 nicotinic receptor subunit: a component of alpha-conotoxin MII-binding nicotinic acetylcholine receptors that modulate dopamine release and related behaviors. J Neurosci 23:11045–11053
Dale HH, Feldberg W, Vogt M (1936) Release of acetylcholine at voluntary muscle motor nerve endings. J Physiol 86:353–380
De Fusco M, Becchetti A, Patrignani A, Annesi G, Ganbardella A, Quattrone A, Ballabio A, Wanke E, Casari G (2000) The nicotinic receptor β2 is mutant in nocturnal frontal lobe epilepsy. Nat Genetics 26:275–276
Deneris ES, Connolly J, Boulter J, Wada E, Wada K, Swanson LW, Patrick J, Heinemann S (1988) Primary structure and expression of β2: A novel subunit of neuronal nicotinic acetylcholine receptors. Neuron 1:45–54
Deneris ES, Boulter J, Swanson LW, Patrick J, Heinemann S (1989) β3: A new member of nicotinic acetylcholine receptor gene family is expressed in brain. J Biol Chem 264:6268–6272
Drisdel RC, Green WN (2000) Neuronal α-bungarotoxin receptors are α7 homomers. J Neurosci 20:133–139
Dwoskin LP, Buxton ST, Jewell AL, Crooks PA (1993) S(−)-Nornicotine increases dopamine release in a calcium-dependent manner from superfused rat striatal slices. J Neurochem 60:2167– 2174
Elgoyhen A, Johnson D, Boulter J, Vetter D, Heinemann S (1994) α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705–715
Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, Boulter J (2001) α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and chochlear mechanosensory hair cells. Proc Natl Acad Sci 98:3501–3506
Fabian-Fine R, Skehel P, Erington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the α7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21:7993–8003
Fambrough DM (1979) Control of acetylcholine receptors in skeletal muscle. Physiol Rev 59: 165–227
Fenster CP, Rains MF, Noerager B, Quick MW, Lester RAJ (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J Neurosci 17:5747–5759
Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV (1998) Synaptic potentials mediated by α-bungarotoxin-sensitive nicotinic receptors in rat hippocampal interneurons. J Neurosci 18:8228–8235
Giorguieff-Chesselet MF, Kemel ML, Wandscheer D, Glowinski J (1979) Regulation of dopamine release by presynaptic nicotinic receptors in rat striatal slices: effect of nicotine in a low concentration. Life Sci 25:1257–1262
Goldman D, Simmons D, Swanson LW, Patrick J, Heinemann S (1986) Mapping of brain areas expressing RNA homologous to two different acetylcholine receptor α-subunits. Proc Natl Acad Sci 83:4076–4080
Gotti C, Moretti M, Clementi F, Riganti L, McIntosh JM, Collins AC (2005) Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion. Mol Pharmacol 67:2007–2015
Gotti C, Zoli M, Clementi F (2006a) Brain nicotinic acetylcholine receptors: native subtypes and their relevance. TIPS 27:482–491
Gotti C, Moretti M, Bohr I, Ziabreva I, Vailati S, Longhi R, Riganti L, Gaimarri A, McKeith IG, Perry RH, Aarsland D, Larsen JP, Sher E, Beattie R, Clementi F, Court JA (2006b) Selective nicotinic acetylcholine receptor subunit deficits identified in Alzheimer's disease, Parkinson's disease and dementia with Lewy bodies by immunoprecipitation. Neurobiol Dis 23:481–489
Gotti C, Moretti M, Gaimarri A, Zanardi A, Clementi F, Zoli M (2007) Heterogeneity and complexity of native brain nicotinic receptors. Biochem Pharmacol 74:1102–1111
Grady SR, Marks MJ, Wonnacott S, Collins AC (1992) Characterization of nicotinic receptormediated [3H]dopamine release from synaptosomes prepared from mouse striatum. J Neurochem 59:848–856
Grady SR, Marks MJ, Collins AC (1994) Desensitization of nicotine-stimulated [3H]dopamine release from mouse striatal synaptosomes. J Neurochem 62:1390–1398
Grady SR, Grun EU, Marks MJ, Collins AC (1997) Pharmacological comparison of transient and persistent [3H]dopamine release from mouse striatal synaptosomes and response to chronic L-nicotine treatment. J Pharmacol Exp Ther 282:32–43
Grady SR, Murphy KL, Cao J, Marks MJ, McIntosh JM, Collins AC (2002) Characterization of nicotinic agonist-induced [3H]dopamine release from synaptosomes prepared from four mouse brain regions. J Pharmacol Exp Ther 301:651–660
Grady SR, Salminen O, Laverty D, Whiteaker P, McIntosh JM, Collins AC, Marks MJ (2007) The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals. Biochem Pharmacol 74:1235–1246
Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716
Heidmann T, Changeux J-P (1978) Structural and functional properties of the acetylcholine receptor in its purified and membrane-bound states. Annu Rev Biochem 47:317–357
Heinemann S, Boulter J, Connolly J, Deneris E, Duvoisin R, Hartley M, Hermans-Borgmeyer I, Hollman M, O-Shea-Greenfield A, Papke R, Rogers S, Patrick J (1991) The nicotinic receptor genes. Clin Neuropharmacol 14:S45–S61
Hogg RC, Bertrand D (2004) Neuronal nicotinic receptors and epilepsy, from genes to possible therapeutic compounds. Bioorganic Med Chem Lett 14:1859–1861
Houghtling RA, Davila-Garcia MI, Kellar KJ (1995) Characterization of (+/•)(•)[3H] epibatidine binding to nicotinic cholinergic receptors in rat and human brain. Mol Pharmacol 48: 280–287
Jones IW, Wonnacott S (2004) Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci 24:11244–11252
Karlin A (2002) Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci 3(2):102–114
Keyser KT, Britto LRG, Schoepfer R, Whiting P, Cooper J, Conroy W, Brozozowska-Prechtl A, Karten HJ, Lindstrom J (1993) Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick brain. J Neurosci 13:442–452
Khiroug S, Harkness PC, Lamb PW, Sudweeks S, Khiroug L, Millar NS, Yakel JL (2002) Rat nicotinic ACh receptor α7 and β2 subunits co-assemble to form functional heteromeric nicotinic receptor channels. J Physiol 540:425–434
Kibjakow AW (1933) Uber humorale ubertragung der erregung von einem neuron auf das andere. Pflugers Arch Ges Physiol 232:423–443
Klassen A, Glykys J, Maguire J, Labarca C, Mody I, Boulter J (2006) Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy. Proc Natl Acad Sci U S A 103:191152–191157
Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21:1452–1463
Kulak JM, Nguyen TA, Olivera BM, McIntosh JM (1997) Alpha-conotoxin MII blocks nicotinestimulated dopamine release in rat striatal synaptosomes. J Neurosci 17:5263–5270
Kuryatov A, Gerzanich V, Nelson M, Olale F, Lindstrom J (1997) Mutation causing autosomal dominant nocturnal frontal lobe epilepsy alters Ca2+ permeability, conductance, and gating of human α4β2 nicotinic acetylcholine receptors. J Neurosci 17:9035–9047
Kuryatov A, Olale FA, Choi C, Lindstrom J (2000) Acetylcholine receptor extracellular domain determines sensitivity to nicotine-induced inactivation. Eur J Pharmacol 393:11–21
Langley JN (1880) On the antagonism of poisons. J Physiol 3:11–21
Langley JN (1890) On the physiology of salivary secretion: Part VI. Chiefly upon the connection of peripheral nerve fibres which run to the sub-lingual and sub-maxillary glands. J Physiol 11:123–158
Langley JN (1901) On the stimulation and paralysis of nerve-cells and of nerve-endings. Part I. J Physiol 27:224–236
Langley JN (1905) On the reaction of cells and of nerve-endings to certain poisons, chiefly as regards the reaction of striated muscle to nicotine and curari. J Physiol 33:374–413
Langley JN (1907) On the contraction of muscle, chiefly in relation to the presence of “receptive” substances. Part I. J Physiol 36:347–384
Langley JN, Dickinson WL (1889) On the local paralysis of peripheral ganglia, and on the connexion of different classes of nerve fibres with them. Proc R Soc 46:423–431
Langley JN, Dickinson WL (1890a) On the progressive paralysis of the different classes of nerve cells in the superior cervical ganglion. Proc R Soc 47:379–390
Langley JN, Dickinson WL (1890b) Pituri and nicotine. J Physiol 11:265–306
Le Novere N, Zoli M, Changeux JP (1996) Neuronal nicotinic receptor alpha 6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur J Neurosci 8: 2428–2439
Leutje CW, Patrick J (1991) Both α- and β-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 11:837–845
Lindstrom J (1998) Purification and cloning of nicotinic acetylcholine receptors. In: Arneric SP, Brioni JD (eds) Neuronal nicotinic receptors: pharmacology and therapeutic opportunities. Wiley, New York, pp 3–23
Lippiello PM, Sears SB, Fernandes KG (1987) Kinetics and mechanism of L-[3H]nicotine binding to putative high affinity receptor sites in rat brain. Mol Pharmacol 31:392–400
Loewi O (1921) Uber humorale Ubertragbarkeit der herznervenwirkung. Pflugers Arch Ges Physiol 189:239–242
Loewi O, Navratil E (1926) Uber humorale ubertragbarkeit der herznervenwirkung. X Mitteilung uber das schicksal das vagusstoffs. Pflugers Arch Ges Physiol 214:678–688
Mansvelder HD, McGehee DS (2000) Long-term potentiation of excitatory imputs to brain reward areas by nicotine. Neuron 27:349–357
Marks MJ, Collins AC (1982) Characterization of nicotine binding in mouse brain and comparison with the binding of α-bungarotoxin and quinuclidinyl benzilate. Mol Pharmacol 22:554–564
Marks MJ, Burch JB, Collins AC (1983) Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J Pharmacol Exp Ther 226:817–825
Marks MJ, Stitzel JA, Romm E, Wehner JM, Collins AC (1986) Nicotinic binding sites in rat and mouse brain: comparison of acetylcholine, nicotine, and alpha-bungarotoxin. Mol Pharmacol 30:427–436
Marks MJ, Campbell SM, Romm E, Collins AC (1991) Genotype influences the development of tolerance to nicotine in the mouse. J Pharmacol Exp Ther 259:392–402
Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, Collins AC (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J Neurosci 12:2765–2784
Marks MJ, Smith KW, Collins AC (1998) Differential agonist inhibition identifies multiple epibatidine binding sites in mouse brain. J Pharmacol Exp Ther 285:377–386
Marks MJ, Whiteaker P, Calcaterra J, Stitzel JA, Bullock AE, Grady SR, Picciotto MR, Changeux JP, Collins AC (1999) Two pharmacologically distinct components of nicotinic receptormediated rubidium efflux in mouse brain require the beta2 subunit. J Pharmacol Exp Ther 289:1090–1103
Marks MJ, Stitzel JA, Grady SR, Picciotto MR, Changeux JP, Collins AC (2000) Nicotinic-agonist stimulated (86)Rb(+) efflux and [(3)H]epibatidine binding of mice differing in beta2 genotype. Neuropharmacology 39:2632–2645
Marks MJ, Whiteaker P, Collins AC (2006) Deletion of the α7, β2 and β4 nicotinic receptor subunit genes identifies highly expressed subtypes with relatively low affinity for [3H]-epibatidine. Mol Pharmacol 70:947–959
Marks MJ, Meinerz NM, Drago J, Collins AC (2007) Gene targeting demonstrates that α4 nicotinic acetylcholine receptor subunits contribute to expression of diverse [3H]epibatidine binding sites and components of biphasic 86Rb+ efflux with high and low sensitivity to stimulation by acetylcholine. Neuropharmacol 53:390–405
Marshall CR (1913) Studies on the pharmaceutical action of tetra-alkyl-ammonium compounds. Trans R Soc Edinb 1:17–40
Marubio LM, del Mar Arroyo-Jimenez M, Condero-Erausquin M, Lena C, Le Novere N, de Kerchove d'Exaerde A, Huchet M, Damaj MI, Changeux JP (1999) Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398:805–810
Miledi R, Potter LT (1971) Acetylcholine receptors in muscle fibers. Nature 233:599–603
Nelson S, Shelton GD, Lei S, Lindstrom JM, Conti-Tronconi BM (1992) Epitope mapping of monoclonal antibodies to Torpedo acetylcholine receptor gamma subunits, which specifically recognize the epsilon subunit of mammalian muscle acetylcholine receptor. J Neuroimmunol 36:13–27
Numa S (1983) Molecular structure of the nicotinic acetylcholine receptor. Cold Spring Harbor Symp Mol Biol 1:57–69
Orr-Urtreger A, Goldner FM, Saeki M, Lorenzo I, Goldberg L, deBiasis M, Dani JA, Patrick JW, Beaudet AL (1997) Mice deficient in the α7 neuronal nicotinic acetylcholine receptor lack α-bungarotoxin binding sites and hippocampal fast nicotinic currents. J Neurosci 17: 9165–9171
Oswald RE, Freeman JA (1981) Alpha-bungarotoxin binding and central nervous system nicotinic acetylcholine receptors. Neuroscience 6:1–14
Pabreza LA, Dhawan S, Kellar KJ (1991) [3H]cytisine binding to nicotinic cholinergic receptors in brain. Mol Pharmacol 39:9–12
Paradiso K, Zhang J, Steinbach JH (2001) The C-terminus of the human nicotinic α4β2 receptor forms a binding site required for potentiation by an estrogenic steroid. J Neurosci 21: 6561–6568
Paton WDM, Zaimis EJ (1949) The pharmacological actions of polymethylene bistrimethylammonium salts. Br J Pharmacol Chemother 4:381–400
Patrick J, Stallcup WB (1977) α-Bungarotoxin binding and cholinergic receptor function on a rat sympathetic nerve line. J Biol Chem 252:8629–8633
Patrick J, Boulter J, Deneris E, Wada K, Wada E, Connolly J, Swanson L, Heinemann S (1989) Structure and function of neuronal nicotinic acetylcholine receptors deduced from cDNA clones. Prog Brain Res 79:27–33
Pauly JR, Collins AC (1993) An autoradiographic analysis of alterations in nicotinic cholinergic receptors following 1 week of corticosterone supplementation. Neuroendocrinology 57: 262–271
Pauly JR, Stitzel JA, Marks MJ, Collins AC (1989) An autoradiographic analysis of cholinergic receptors in mouse brain. Brain Res Bull 22: 453–459
Pauly JR, Grun EU, Collins AC (1990a) Chronic corticosterone administration modulates nicotine sensitivity and brain nicotinic receptor binding in C3H mice. Psychopharmacology 101: 310–316
Pauly JR, Ullman EA, Collins AC (1990b) Strain differences in adrenalectomy-induced alterations in nicotine sensitivity in the mouse. Pharmacol Biochem Behav 35: 171–179
Pauly JR, Marks MJ, Gross SD, Collins AC (1991) An autoradiographic analysis of cholinergic receptors in mouse brain after chronic nicotine treatment. J Pharmacol Exp Ther 258: 1127–1136
Perry DC, Kellar KJ (1995) [3H]epibatidine labels nicotinic receptors in rat brain: an autoradiographic study. J Pharmacol Exp Ther 275:1030–1034
Perry WLM, Talesnik J (1953) The role of acetylcholine in synaptic transmission at parasympathetic ganglia. J Physiol 119:455–469
Phillips HA, Favre I, Kilpatrick M, Zuberi SM, Goudie D, Heron SE, Scheffer IE, Sutherland GR, Berkovic SF, Bertrand D, Mulley JC (2001) CHRNB2 is the second acetylcholine receptor subunit associated with autosomal dominant nocturnal frontal lobe epilepsy. Am J Hum Genet 68:225–231
Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, LeNovere N, Vincent E, Pich EM, Brulet P, Changeux JP (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotinic receptor in the brain. Nature 374:65–67
Porter JT, Cauli B, Tsuzuki K, Lambolez P, Rossier J, Audinet E (1999) Selective excitation of subtypes of neocortical inmterneurons by nicotinic receptors. J Neurosci 19:5228–5235
Pugh PC, Corriveau RA, Conroy WG, Berg DK (1995) Novel subpopulation of neuronal acetylcholine receptors among those binding α-bungarotoxin. Mol Pharmacol 47:717–725
Quik M, Sum JD, Whiteaker P, McCallum SE, Marks MJ Musachio J, McIntosh JM, Collins AC, Grady SR (2003) Differential declines in striatal nicotinic receptor subtype function after nigrostriatal damage in mice. Mol Pharmacol 63:1169–1179
Quik M, Vailati S, Bordia T, Kulak JM, Fan H, McIntosh JM, Clementi F, Gotti C (2005) Subunit composition of nicotinic receptors in monkey striatum: effect of treatments with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine or l-DOPA. Mol Pharmacol 67:32–41
Raftery MA, Hunkapiller MW, Strader CD, Hood LE (1980) Acetylcholine receptor: complex of homolygous subunits. Science 208:1454–1457
Rapier C, Lunt GG, Wonnacott S (1988) Stereoselective nicotine-induced release of dopamine from striatal synaptosomes: concentration dependence and repetitive stimulation. J Neurochem 50:1123–1130
Rodriguez-Pinguet NO, Pinguet TJ, Figl A, Lester HA, Cohen BN (2005) Mutations linked to autosomal dominant nocturnal frontal lobe epilepsy affect allosteric Ca2+ activation of the α4β2 nicotinic acetylcholine receptor. Mol Pharmacol 68:487–501
Romano C, Goldstein A (1980) Stereospecific nicotine receptors on rat brain membranes. Science 210:647–650
Rush R, Kuryatov A, Nelson ME, Lindstrom J (2002) First and second transmembrane segments of α3, α4, β2 and β4 nicotinic acetylcholine receptor subunits influence the efficacy and potency of nicotine. Mol Pharmacol 61:1416–1422
Sabey K, Paradiso K, Zhang J, Steinbach JH (1999) Ligand binding and activation of rat nicotinic α4β2 receptors stably expressed in HEK293 cells. Mol Pharmacol 55:58–66
Salminen O, Murphy KL, McIntosh JM, Drago J, Marks MJ, Collins AC, Grady SR (2004) Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 65:1526–1535
Salminen O, Whiteaker P, Grady SR, Collins AC, McIntosh JM, Marks MJ (2005) The subunit composition and pharmacology of α-conotoxin MII-binding nicotinic acetylcholine receptors studied by a novel membrane-binding assay. Neuropharmacology 48:696–705
Salminen O, Drapeau J, McIntosh JM, Collins AC, Marks MJ, Grady SR (2007) Pharmacology of α-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol 71:1563–1571
Saragoza PA, Modir JG, Goel N, French KL, Li L, Nowak MW, Stitzel JA (2003) Identification of an alternatively processed nicotinic receptor α7 subunit mRNA in mouse brain. Mol Brain Res 117:15–26
Schoepfer R, Conroy WG, Whiting P, Gore M, Lindstrom J (1990) Brain α-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5:35–48
Schmidt J (1988) Biochemistry of nicotinic acetylcholine receptors in the vertebrate brain. Int Rev Neurobiol 30:1–38
Schwartz RD, McGee R Jr, Kellar KJ (1982) Nicotinic cholinergic receptors labeled by [3H]acetylcholine in rat brain. Mol Pharmacol 22:56–62
Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. J Neurosci 13:596–604
Severance EG, Cuevas J (2004) Distribution and synaptic localization of nicotinic acetylcholine receptors containing a novel alpha7 subunit isoform in embryonic rat cortical neurons. Neurosci Lett 372:104–109
Sgard F, Charpantier E, Bertrand S, Walker N, Caput D, Graham D, Bertrand D, Besnard F (2002) A novel human nicotinic receptor subunit, α10, that confers functionality to the α9-subunit. Mol Pharmacol 61:150–159
Sharples CG, Kaiser S, Soliakov L, Marks MJ, Collins AC, Washburn M, Wright E, Spencer JA, Gallagher T, Whiteaker P, Wonnacott S (2000) UB-165: a novel nicotinic agonist with subtype selectivity implicates the alpha4beta2* subtype in the modulation of dopamine release from rat striatal synaptosomes. J Neurosci 20:2783–2791
Steinlein OK (2007) Genetic disorders caused by mutated acetylcholine receptors. Life Sci 80:2186–2190
Steinlein OK, Mulley JC, Propping P, Wallace RH, Phillips HA, Sutherland GR, Scheffer IE, Berkovic SF (1995) A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat Genet 11:201–203
Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine's defensive function in nature. PloS Biol 2:1074–1080
Sudweeks SN, Yakel JL (2000) Functional and molecular characterization of neuronal ACh receptors in rat CA1 hippocampal neurons. J Physiol 527:515–528
Teper Y, Whyte D, Cahir E, Lester HA, Grady SR, Marks MJ, Cohen BN, Fonck C, McClure-Begley T, McIntosh JM, Labarca C, Lawrence A, Chen F, Gantois I, Davies PJ, Petrou S, Murphy M, Waddington J, Horne MK, Berkovic SF, Drago J (2007) Nicotine-induced dystonic arousal complex in a mouse line harboring a human autosomal-dominant nocturnal frontal lobe epilepsy mutation. J Neurosci 27:10128–10142
Wada K, Ballivet M, Boulter J, Connolly J, Wada E, Deneris ES, Swanson LW, Heinemann S, Patrick J (1988) Functional expression of a new pharmacological subtype of brain acetylcholine receptor. Science 240:330–334
Weiland S, Bertrand D, Leonard S (2000) Neuronal nicotinic acetylcholine receptors: from the gene to the disease. Behav Brain Res 113:43–56
Whiteaker P, Marks MJ, Grady SR, Lu Y, Picciotto MR, Changeux J-P, Collins AC (2000) Pharmacological and null mutation approaches reveal nicotinic receptor diversity. Eur J Pharmacol 393:123–135
Whiteaker P, Peterson CG, Xu W, McIntosh JM, Paylor R, Beaudet AL, Collins AC, Marks MJ (2002) Involvement of the alpha3 subunit in central nicotinic binding populations. J Neurosci 22:2522–2529
Wu J, George AA, Schroeder KM, Xu L, Marxer-Miller S, Lucero L, Lukas RJ (2004) Electrophysiological, pharmacological, and molecular evidence for alpha7-nicotinic acetylcholine receptors in rat midbrain dopamine neurons. J Pharmacol Exp Ther 311:80–91
Xu J, Ferraro NV, Zhu Y, Fonck C, Deshpande P, Marks MJ, Collins AC, Lester HA, Heinemann SF (2006) Increased sensitivity to nicotine-induced seizures in β2 V287L knock-in mice. Soc Neurosci Abstr 36:326.314/C382
Yu CR, Role LW (1998a) Functional contribution of the α7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones. J Physiol 509:651–665
Yu CR, Role LW (1998b) Functional contribution of the α5 subunit to neuronal nicotinic channels expressed by chick sympathetic ganglion neurones. J Physiol 509:667–681
Zhang J, Berg DK (2007) Reversible inhibition of GABAA receptors by α7-containing nicotinic receptors on the vertebrate postsynaptic neurons. J Physiol 579.3:753–763
Zhou Y, Nelson ME, Kuryatov A, Choi C, Cooper J, Lindstrom J (2003) Human alpha4beta2 acetylcholine receptors formed from linked subunits. J Neurosci 23:9004–9015
Zoli M, Clement L, Picciotto MR, Changeux J-P (1998) Identification of four classes of brain nicotinic receptors using β2 mutant mice. J Neurosci 18:4461–4472
Zoli M, Moretti M, Zanardi A, McIntosh JM, Clementi F, Gotti C (2002) Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J Neurosci 22:8785–8789
Zwart R, Vijverberg HP (1998) Four pharmacologically distinct subtypes of alpha4beta2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Mol Pharmacol 54:1124–1131
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Collins, A.C., Salminen, O., Marks, M.J., Whiteaker, P., Grady, S.R. (2009). The Road to Discovery of Neuronal Nicotinic Cholinergic Receptor Subtypes. In: Henningfield, J.E., London, E.D., Pogun, S. (eds) Nicotine Psychopharmacology. Handbook of Experimental Pharmacology, vol 192. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-69248-5_4
Download citation
DOI: https://doi.org/10.1007/978-3-540-69248-5_4
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-69246-1
Online ISBN: 978-3-540-69248-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)