Abstract
Nicotinic acetylcholine receptors on neurons are part of a gene family that includes nicotinic acetylcholine receptors on skeletal muscles and neuronal αbungarotoxin-binding proteins that in many species, unlike receptors, do not have an acetylcholine-regulated cation channel. This gene superfamily of ligand-gated receptors also includes receptors for glycine and gamma-aminobutyric acid. Rapid progress on neuronal nicotinic receptors has recently been possible using monoclonal antibodies as probes for receptor proteins and cDNAs as probes for receptor genes. These studies are the primary focus of this review, although other aspects of these receptors are also considered.
In birds and mammals, there are subtypes of neuronal nicotinic receptors. All of these receptors differ from nicotinic receptors of muscle pharmacologically (none bind αbungarotoxin, and some have very high affinity for nicotine), structurally (having only two types of subunits rather than four), and, in some cases, in functional role (some are located presynaptically). However, there are amino acid sequence homologies between the subunits of these receptors that suggest the location of important functional domains.
Sequence homologies also suggest that the subunits of the proteins of this family all evolved from a common ancestral protein subunit. The ligand-gated ion channel characteristic of this superfamily is formed from multiple copies of homologous subunits. Conserved domains responsible for strong stereospecific association of the subunits are probably a fundamental organizing principle of the superfamily. Whereas the structure of muscle-type nicotinic receptors appears to have been established by the time of elasmobranchs and has evolved quite conservatively since then, the evolution of neuronal-type nicotinic receptors appears to be in more rapid flux.
Certainly, the studies of these receptors are in rapid flux, with the availability of monoclonal antibody probes for localizing, purifying, and characterizing the proteins, and cDNA probes for determining sequences, localizing mRNAs, expressing functional receptors, and studying genetic regulation.
The role of nicotinic receptors in neuromuscular transmission is well understood, but the role of nicotinic receptors in brain function is not. The current deluge of data using antibodies and cDNAs is beginning to come together nicely to describe the structure of these receptors. Soon, these techniques may combine with others to better reveal the functional roles of neuronal nicotinic receptors.
Similar content being viewed by others
Abbreviations
- ACh:
-
Acetylcholine
- AChR:
-
Aceylcholine receptor
- BAC:
-
Bromoacetylcholine
- αBgt:
-
αBungarotoxin
- cDNA:
-
Complementary DNA
- DTT:
-
Dithiothreitol
- GABA:
-
Gamma amino butyric acid
- mAb:
-
Monoclonal antibody
- MBTA:
-
4-(N-Maleimido)-benzyltrimethylammonium iodide
- MIR:
-
Main immunogenic region
- mw:
-
Molecular weight
- βNGF:
-
Nerve growth factor, β subunit
References
Abood L., Lagone J., Bjercke R., Lu X., Banerjee S. (1987) Characterization of a purified nicotinic receptor from rat brain by using idiotypic and anti-idiotypic antibodies.PNAS USA 84; 6587–6590.
Abood L., Latham W., and Grassi S. (1983) Isolation of a nicotinic binding site from rat brain by affinity chromatography.Proc. Natl. Acad. Sci. (PNAS) USA 80; 3536–3539.
Aceto M. and Martin B. (1982) Central actions of nicotine.Med. Res. Rev. 2; 43–62.
Albuquerque E. X., Barnard E. A., Chiu T. H., Lapa A. J., Dolly J. O., Jansson S. E., Daly J. W., and Witkop B. (1973) Acetylcholine receptor and ion conductance modulator sites at the murine neuromuscular junction: evidence from specific toxin reactions.PNAS USA 70; 949–953.
Anderson D. and Blobel G. (1983) Molecular events in the synthesis and assembly of nicotinic acetylcholine receptor.Cold Spring Harbor Symposium XLVIII; 125–134.
Aracava Y., Deshpande S., Swanson K., Rapoport A., Wonnacott S., Lunt G., and Albuquerque E. (1987) Nicotinic acetylcholine receptors in cultured neurons from the hippocampus and brain stem of the rat characterized by single channel recording.FEBS Lett. 222; 63–70.
Arriza J., Weinberger C., Cerelli G., Glaser T., Handelin B., Housman D., and Evans R. (1987) Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor.Science 237; 268–275.
Baizer L. and Weiner N. (1985) Nerve growth factor treatment enhances nicotine-stimulated dopamine release and increses in cyclic adenosine 3′: 5′ monophosphate levels in PC12 cell cultures.J. Neurosci. 5; 1176–1179.
Balfour D. (1982) The effects of nicotine on brain neurotransmitter syistems.Pharm. Ther. 16; 269–282.
Ballivet M., Patrick J., Lee J., and Heinemann S. (1982) Molecular cloning of cDNA coding for the g subunit ofTorpedo acetylcholine receptor.PNAS USA 79; 4466–4470.
Barkas T., Mauron A., Roth B., Alliod C., Tzartos S., and Ballivet M. (1987) Mapping the main immunogenic region and toxin binding site of the nicotinic acetylcholine receptor.Science 235; 77–80.
Barnard E., Beeson D., Cockcroft V., Darlison M., Hicks A., Lai F. A., Moss S., and Squire M. D. (1986) Molecular biology of nicotinic acetylcholine receptors from chicken muscle and brain.Nicotinic Acetylcholine Receptor, series H, vol. 3, Maelicke A., ed., NATO ASI Series, Springer-Verlag, Heidelberg, pp. 389–415.
Barnard E. Darlison M., and Seeburg P. (1987) Molecular biology of the GAGAA receptor: the receptor/channel superfamily.TINS 10: 502–509.
Benowitz N. (1986) Clinical pharmacology of nicotine.Ann. Rev. Med. 37: 21–32.
Berg D., Jacob M., Margiotta J., Nishi R., Stollberg J., Smith M., and Lindstrom J. (1985) Cholinergic development and identification of synaptic components for chick ciliary ganglion neurons in cell culture.Molecular Basis of Neural Development, Edelman G., Gall W., and Cowan W., eds., Wiley, New York.
Betz H. (1981) Characterization of the αbungarotoxin receptor in chick embryo retina.Eur. J. Biochem. 117; 131–139.
Betz H. and Pfeiffer F. (1984) Monoclonal antibodies against the αbungarotixin binding protein of chick optic lobe.J. Neurosci. 4; 2095–2105.
Betz H., Graham D., and Rehm H. (1982) Identification of polypeptides associated with a putative neuronal nicotinic acetylcholine receptor.J. Biol. Chem. 257; 11390–11394.
Blatt Y., Montal M., Lindstrom J., and Montal M. (1986) Monoclonal antibodies directed against epitopes in the β and ψ subunits of theTorpedo cholinergic receptor affect channel gating.J. Neurosci. 6; 481–486.
Block G. A. and Billiar R. B. (1979) Immunologic similarities between the hypothalmic abungarotoxin receptors and theTorpedo californica nicotinic cholinergic receptor.Brain Res 178; 381–387.
Blount P. and Merlie J. (in press) Native folding of an acetylcholine receptor a subunit expressed in the absence of other receptor subunits.J. Biol. Chem.
Boulter J., Connolly J., Deneris E., Goldman D., Heinemann S., and Patrick J. (in press) Functional expression of two neuronal nictinic acetylcholine receptors from cDNA clones identifies a gene family.PNAS. USA.
Boulter J., Evans K., Goldman D., Martin D., Treco D., Heinemann S., and Patrick J. (1986a) Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor a subunit.Nature 319; 368–374.
Boulter J., Evans K., Martin G., Mason P., Stengelin S., Goldman D., Heinemann S., and Patrick J. (1986b) Isolation and sequence of cDNA clones coding for the precursor to the ψ subunit of mouse muscle nicotinic acetylcholine receptor.J. Neurosci. Res. 16; 37–49.
Boulter J., Luyten W., Evans K., Mason P., Ballivet M., Goldman D., Stengelin S., Martin G., Heinemann S., and Patrick J. (1985) Isolation of a clone coding for the α subunit of a mouse acetylcholine receptor.J. Neurosci. 5; 2545–2552.
Bradley P. B., and Dray A. (1972) Short latency excitation of brain stem neurones in the rat by acetylcholine.Brit. J. Pharmacol. 4; 372–374.
Breer H., and Benke D. (1986) Messenger RNA from insect nervous tissue induces expression of neuronal acetylcholine receptors inXenopus oocytes.Mol. Brain Res. 1; 111–117.
Breer H., Hinz G., Madler U., and Hanke W. (1986) Identification and reconstitution of a neuronal acetylcholine receptor from insects.Nicotinic Acetylcholine Receptor, vol. 3, Maelicke A., ed., NATO ASI Series H, Springer-Verlag, Heidelberg., pp. 319–332.
Breer R., Kleene R., and Benke D. (1984) Isolation of a putative nicotinic acetylcholine receptor from the central nervous system ofLocusta migratoria.Neurosci. Lett. 4; 323–328.
Breer H., Kleene R., and Hinz G. (1985) Molecular forms and subunit structure of the acetylcholine receptor in the central nervous system of insects.J. Neurosci. 5; 3386–3392.
Brisson A., and Unwin P. (1985) Quaternary structure of the acetylcholine receptor.Nature 315; 474–477.
Brown D. A., Docherty R. J., and Halliwell J. V. (1983) Chemical Transmission in the rat interpeduncular nucleus in vitro.J. Physiol. (Lond.) 353; 101–109.
Buonanno A., Mudd J., Shah V., and Merlie J. P. (1986) A universal oligonucleotide probe for acetylcholine receptor genes.J. Biol. Chem. 261; 16451–16458.
Carbonetto S. T., Fambrough D. M., and Muller K. J. (1978) Non-equivalence of αbungarotoxin receptors and acetylcholine receptors in chick sympathetic neurons.PNAS USA 75; 1016–1020.
Changeux J-P., Pinset C., and Ribera A. (1986) Effects of chlorpromazine and phencyclidine on mouse C2 acetylcholine receptor kinetics.J. Physiol. 378; 497–513.
Chase B., Holliday J., Reese J., Chun L., and Hawrot E. (1987) Monoclonal antibodies with defined specificities forTorpedo nicotinic acetylcholine receptor cross-react withDrosophila neural tissue.Neurosci. 21; 959–976.
Chiappinelli V. A. (1983) Kappa toxin: a probe for neuronal nicotinic receptor in the avian ciliary ganglion.Brain Res. 277; 9–21.
Chiappinelli V. A. (1985) Actions of snake venom toxins on neuronal nicotinic receptors and other neuronal receptors.Pharm. Ther. 31; 1–32.
Chiappinelli V. A. and Lee J. C. (1985) Kappa-bungarotoxin: self association of a neuronal nicotinic receptor probe.J. Biol. Chem. 260; 6182–6168.
Chiappinelli V. A. and R. E. Zigmond (1987) αBungarotoxin blocks nicotinic transmission in the avian ciliary ganglion.PNAS USA 75; 2999–3003.
Clarke P., Hamill G., Nadi N., Jacobowitz D., and Pert A. (1986) [3H]-Nicotine and [125I] αbungarotoxin-labeled nicotinic receptors in the interpeduncular nucleus of rats. Effects of habenular differentiation.J. Comp. Neurol. 251, 407–413.
Clarke P., Hommer D. W., Pert A., and Skirboll L. R. (1985a) Electrophysiological actions of nicotine onsubstantia nigra single units.Brit. J. Pharm. 8; 827–835.
Clarke P., Schwartz, R. D., Paul S. M., Pert C. B., and Pert A. (1985b) Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]αbungarotoxin.J. Neurosci. 5; 1307–1315.
Claudio T. (1986a) Establishing a system for the stable expression ofTorpedo acetylcholine receptors.Nicotinic Acetylcholine Receptor Structure and Function, Maelicke A., ed,. NATO ASI series H, vol. 3., pp. 431–435.
Claudio T. (1986b) Recombinant DNA technology in the study of ion channelsTrends in Pharm. 7; 308–312.
Claudio T. (1987) Stable expression of transfectedTorpedo acetylcholine receptor α subunits in mouse fibroblast L cells.PNAS USA 84; 5967–5971
Claudio T., Ballivet M., Patrick J., and Heinemann S. (1983) Nucleotide and deduced amino acid sequences ofTorpedo californica acetylcholine receptor ψ subunit.PNAS USA 80; 1111–1115.
Cobbett P., Mason W. T., and Poulain D. A. (1986) Intracellular analysis of control of supraoptic neurone (SON) activity in vitro by acetylcholine (ACh).J. Physiol. (Lond.) 371; 216 P.
Collerton D. (1986) Cholinergic function and interllectual decline in Alzheimer’s disease.Neurosci.19(1); 1–28.
Conti-Tronconi B. M., Dunn S. M. J., Barnard E. A., Dolly J. O., Lai F. A., Ray N., and Raftery M. A. (1985) Brain and muscle nicotinic acetylcholine receptors are different but homologous proteins.PNAS USA 82; 5208–5212.
Cox K. H., DeLeon D., Angerer L., and Angerer R. C. (1984) Detection of mRNAs in sea urchin embryos byin situ hybridization using symmetric RNA probes.Devel. Biol. 101; 485–502.
Criado M., Hochschwender S., Sarin V., Fox J. L. and Lindstrom J. (1985) Evidence for unpredicted transmembrane domains in acetylcholine receptor subunits.PNAS USA 82; 2004–2008.
Criado M., Sarin V., Fox J. L., and Lindstrom J. (1985) Structural localization of the sequence α235–242 of the nicotinic acetylcholine receptor.Biochem. Biophys. Res. Commun. (BBRC) 128; 864–871.
Criado M., Sarin V., Fox J. L. and Lindstrom J. (1986) Evidence that the acetylcholine binding site is not formed by the sequence α127–143 of the acetylcholine receptor.Biochemistry 25; 2839–2846.
Culver P., Fenical W., and Taylor P. (1984) Lophotoxin irreversibly inactivates the nicotinic acetylcholine receptor by preferential association at one of the two primary agonist sites.J. Biol. Chem. 259; 3763–3770.
Curtis D. R. and Ryall R. W. (1966) The synaptic excitation of Renshaw cells.Exp. Brain Res. 2; 81–96.
Dam M. and London E. (1983) Effects of cholinomimetics on glucose utilization in brain optic system.Eur. J. Pharmacol. 87; 137–140.
Damle V. and Karlin A. (1978) Affinity labeling of one of two α-neurotoxin binding sites in acetylcholine receptor fromTorpedo californica.Biochemistry 1; 2039–2045.
Damle V., McLaughlin M., and Karlin A. (1978) Bromoacetylcholine as an affinity label of the acetylcholine receptor fromTorpedo californica.BBRC 84; 845–851.
De Belleroche J., Lugmani Y., and Bradford H. (1979) Evidence for presynaptic cholinergic receptors on dopaminergic terminals: degeneration studies with 6-hydroxydopamine.Neurosci. Letts. 11; 209–213.
Deneris E., Boulter J., Copnnolly J., Wada K., Patrick J., and Heinemann S. (1987) Identification of a non-alpha subunit of neuronal nicotinic receptors.Neuroscience Soc. Abstr. 260.11.
Desan P., Gruberg E., Grewell K., and Eckenstein F. (1987) Cholinergic innervation of the optic tectum in the frogRana pipiens.Brain Res. 413; 344–349.
Devillers-Thiery A., Giraudat J., Bentaboulet M., and Changeux J-P. (1983) Complete mRNA coding sequence of the α subunit ofTorpedo marmorata acetylcholine receptor: a model for the transmembrane organization of the polypeptide chain.PNAS USA 80; 2067–2071.
Dichter M. A., Tischler A. S., and Greene L. A. (1977) Nerve growth factor-induced increase in electrical excitability and acetylcholine sensitivity of a rat pheochromocytoma cell line.Nature 268; 501–504.
Dilsaver S. (1986) Cholinergic mechanisms in depression.Brain Res. Rev. 11; 285–316.
Dixon R., Kobilka B., Strader D., Benovic J., Dohlman H., Frielle T., Bolanowski M., Bennett C., Rands E., Diehl R., Mumford R., Slater E., Sigal J., Caron M., Lefkowitz R., and Strader C. (1986) Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsin.Nature 321; 75–79.
Dodson B., Braswell L., and Miller K. (1987) Barbiturates bind to an allosteric regulatory site on nicotinic acetylcholine receptor-rich membranes.Molec. Pharmacol. 32; 119–126.
Downward J., Yarden Y., Mayes E., Scraci G., Totty N., Stockwell P., Ullrich A., Schlessinger J., and Waterfield M. (1984) Close similarity of epidermal growth factor receptor and V-erb-B oncogene protein sequences.Nature 307; 521–527.
Drachman D., Pestronk A., and Stanley E. (1982) Neurotrophic interactions between nerves and muscles: role of acetylcholine.Disorders of the Motor Unit, Schotland D., ed., Wiley, New York,
Dudai Y. (1978) Properties of an αbungarotoxin binding cholinergic nicotinic receptor fromDrosophila melanogaster.Biochim. Biophys. Acta 539; 505–517.
Duggan A. W., Hall J. G. and Lee C. Y. (1976) αBungarotoxin, cobra neurotoxin, and excitation of Renshaw cells by acetylcholine.Brain Res. 107; 166–170.
Egan T. M. and North R. A. (1986) Actions of acetylcholine and nicotine on rat coeruleus neurons in vitro.Neurosci. 19; 565–571.
Eiden L. W., Giraud P., Dave J. R., Hotchkiss A. J., and Affolter H. V. (1984) Nicotinic receptor stimulation activates enkephalin release and biosynthesis sy adrenal chromafin cells.Nature 312; 661–663.
Eldefrawi M. E., Eldefrawi A. T., and O’Brien R. D. (1971) Binding of five cholinergic ligands to housefly brain andTorpedo electroplax.Mol. Pharmacol. 7; 104–110.
Evans S., Goldman D., Heinemann S., and Patrick J. (1987) Muscle acetylcholine receptor biosynthesis: regulation by transcript availability.J. Biol. Chem. 262; 4911–4916.
Evers A., Berkowitz B., and Avignon D. (1987) Correlation between the anesthetic effect of halothane and saturable binding in brain.Nature 328; 157–160.
Fambrough D. (1979) Control of acetylcholine receptors in skeletal muscle.Physiol. Rev. 59; 165–227.
Fels G., Breer H., and Maelicke A. (1983) Are there nicotinic acetylcholine receptors in invertebrate ganglionic tissue?Toxins as Tools in Neurochemistry, Huch F. and Ovchinnikov Y. A., eds., W. de Gruyter, Berlin.
Filbin M. T., G. G. Lunt, and J. F. Donnellan (1983) Partial purification and characterization of an acetylcholine receptor with nicotinic properties from the suraoesophageal ganglion of the locusSchistocerca gregaria.Eur. J. Biochem. 132; 151–156.
Finer-Moore J. and Stroud R. (1984) Amphipathic analysis and possible formation of the ion channel in an acetylcholine receptor.PNAS USA 81; 155–159.
Flynn D. D. and Marsh D. C. (1986) Characterization of L-3H nicotine binding in human cerebral cortex: comparison between Alzheimer’s disease and the normal.J. Neurochem. 47; 1948–1954.
Freeman J. A., Schmidt J. T., and Oswald R. E. (1980) Effect of αbungarotoxin in retinotectal synaptic transmission in goldfish and toad.Neurosci. 5; 929–942.
Frosch M., Phillips E., Aizenman D., Tanck D., and Lipton S. (1986) Nicotinic cholinergic blocking agents enhance process outgrowth by solitary rat retinal ganglion cells in culture.Neurosci. Soc. Mtg. Abstr. 4007. 9.
Fujita N., Nelson N., Fox T., Claudio T., Lindstrom J., Reizman H., and Hess G. (1986) Biosynthesis of theTorpedo californica acetylcholine receptor α subunit in yeast.Science 231; 1284–1287.
Fujita N., Sweet M., Fox T. Nelson N., Claudio T., Lindstrom J., and Hess G. (in press) Expression of cDNAs for acetylcholine receptor subunits in yeast cell lasma membrane.Biochem. J.
Gershoni J. M. (1987) Expression of the αbungarotixin binding site of the nicotinic acetylcholine receptor byEscherichia coli transformants.PNAS USA 84; 4318–4321.
Gershoni J., Hawrot E., and Lentz T. (1983) Binding of αbungarotoxin to isolated α subunit of the acetylcholine receptor ofTorpedo californica: quantitative analysis with protein blots.PNAS USA 80; 4973–4977.
Giorguieff-Chesselet M. F., Kemel M. L., Wandscheer D., and 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.
Giraudat J., Dennis M., Heidmann T., Chang J., and Changeux J-P. (1986) Structure of the high-affinity binding site for noncompetitive blockers of the acetylcholine receptor: serine 262 of the δ subunit is labeled by [3H]chlorpromazine.PNAS USA 83; 2719–2723.
Goldman D., Deneris E., Luyten W., Kochhar A., Patrick J., and Heinemann S. (1987) Members of a nicotinic acetylcholine receptor gene family are expressed in different regions of the mammalian central nervous system.Cell 48; 965–973.
Goldman D., Simmons D., Swanson L., Patrick J., and Heinemann S. (1986) Mapping of brain areas expressing RNA homologous to two different acetylcholine receptor α subunit cDNAs.PNAS USA 83; 4076–4080.
Gotti C., Omini C., Berti F., and Clementi F. (1985) Isolation of a polypeptide from the venom ofBungarus multicinctus that binds to ganglia and blocks the ganglionic transmission in mammals.Neurosci. 15; 563–575.
Grant G. A. and Chiappinelli V. A. (1985) Kappabungarotoxin complete amino acid sequence of a neuronal nicotinic receptor probe.Biochem. 24; 1532–1537.
Greenberg M. E., Ziff E. B., and Greene L. A. (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription.Science 234; 80–83.
Greene L. A., Sytkowski A. J., Vogel Z., and Nisenberg M. W. (1973) αBungarotoxin used as a probe for acetylcholine receptors of cultured neurons.Nature 243; 163–166.
Grenningloh G., Rienitz A., Schmitt B., Methfessel C., Zensen M., Beyreuth K., Gundelfinger E., and Betz H. (1987) The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors.Nature 328; 215–220.
Grunwald F., Schrock H., and Kuschinsky W. (1987) The effect of an acute nicotine infusion on the local cerebral glucose utilization of the awake rat.Brain Res. 400; 232–238.
Gundelfinger E. D., Hermnas-Borgmeyer I., Zopf D., Sawruk E., and Betz H. (1986) Characterization of the mRNA and the gene of a putative neuronal nicotinic acetylcholine receptor protein fromDrosophila, Nicotinic Acetylcholine Receptor, Maelicke A., ed.,NATO ASI Series H, vol. 3, Springer-Verlag, Heidelberg, pp. 437–446.
Guy R. (1983) A structural model of the acetylcholine receptor channel based on partition energy and helix packing calculation.Biophys. J. 45; 249–261.
Halvorsen S. W. and D. K. Berg (1986) Identification of a nicotinic acetylcholine receptor on neurons using an αneurotoxin that blocks receptor function.J. Neurosci. 6; 3405–3412.
Halvorsen S. W. and D. K. Berg (1987) Affinity labeling of neuronal acetylcholine receptor with an αneurotoxin that blocks receptor function.J. Neurosci.7; 2547–2555.
Hamilton S., Pratt D., and Eaton D. (1985) Arrangment of the subunits of the nicotinic acetylcholine receptor ofTorpedo californica as determined by a neurotoxin crosslinking.Biochemistry 24; 2210–2219.
Hanke W. and Breer H. (1986) Channel properties of an insect neuronal acetylcholine receptor protein reconstituted into planar lipid bilayers.Nature 321; 171–174.
Hanke W. and Breer H. (in press) Characterization of the channel properties of a neuronal acetylcholinereceptor reconstituted into planar lipid bilayers.J. Gen. Physiol.
Henley J., Mynlieff M., Lindstrom J., and Oswald R. (1986a) Interaction of monoclonal antibodies to electroplaque acetylcholine receptors with the αbungarotoxin binding site of goldfish brain.Brain Res. 364; 4005–4008.
Henley J., Lindstrom J., and Oswald R. (1986b) Acetylcholine receptor systhesis in retina and transport to the optic tectum in goldfish.Science 232; 1627–1629.
Henley J., Lindstrom J., and Oswald R. (1987) Interaction of monoclonal antibodies with αbungarotoxin and (-) nicotine binding sites in goldfish brain: identification of two nicotinic acetylcholine receptor subtype.EMBO J. 5; 1503–1508.
Henley J. M., and Oswald R. E. (1987) Two distinct (-) nicotine binding sites in goldfish brain.J. Biol. Chem. 262; 6691–6698.
Hermans-Borgmeyer I., Zopf D., Ryseck R-P., Hovemann B., Betz H., and Gundelfinger E. D. (1986) Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein fromDrosophila.EMBO J. 5; 1503–1508.
Higgins L. S. and Berg D. K. (1987) Immunological identification of a nicotinic acetylcholine receptor on bovine chromaffin cells.J. Neurosci. 7; 1792–1798.
Hinton D., Sadun A., Blanks J., and Miller C. (1986) Optic nerve degeneration in Alzheimer’s disease.New Engl. J. Med. 315; 485–487.
Hucho F., Oberthur W., Lottspeich F. (1986) The ion channel of the nicotinic acetylcholine receptor is formed by the homologous helices MII of the receptor subunits.FEBS Letts. 205; 137–142.
Huganir R., Delcour A., Greengard P., and Hess G. (1986) Phosphorylation of the nicotinic acetylcholine receptor regulates its rate of desensitization.Nature 321; 774–777.
Hunt S. and Schmidt J. (1978) Some observations on the binding patterns of αbungarotoxin in the central nervous system of the rat.Brain Res. 157; 213–232.
Ikeda H. and Sheardown M. J. (1982) Acetylcholine may be an excitatory transmitter mediating visual excitation of ‘transient’ cells with the periphery affect in the cat retina: iontophoretic studies in vivo.Neurosci. 7; 1299–1308.
Imamura K. and T. Kasamatsu (1986) Noradrenergic and cholinergic interaction in ocular dominance plasticity.Neurosci. Soc. Mtg. Abstr. 373.97
Imoto K., Methfessel C., Sakmann B., Mishina M., Mori Y., Konno T., Fukuda K., Kurasaki M., Bujo H., Fujita Y. Y., and Numa S. (1986) Location of a α subunit region determining ion transport through the acetylcholine receptor channel.Nature,324; 670–674.
Jacob M. and Berg D. (1983) The ultra structural localization of αbungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons.J. Neurosci. 3; 260–271.
Jacob M., Berg D., and Lindstrom J. (1984) A shared antigenic determinant between the Electrophorus acetylcholine receptor and a synaptic component on chick ciliary ganglion neurons.PNAS USA 81; 3223–3227.
Jacob M., Lindstrom J., and Berg D. (1986) Surface and intracellular distribution of a putative neuronal nicotinic acetylcholine receptor.J. Cell Biology 103; 205–214.
Kao P., Dwork A., Kaldany R., (1984) Identification of the α subunit half cysteine specifically labeled by an affinity reagent for the acetylcholine receptor binding site.J. Biol. Chem. 259; 11662–11665.
Kao P., and Karlin A. (1986) Disulfide crosslink between adjacent half-cystinyl residues at the acetylcholine binding site.Biophys. J. 49; 5a.
Karlin A. (1980) Molecular properties of nicotinic acetylcholine receptors.The Cell Surface and Neuronal Function, Poste G., Nicolson G., and Cotman C., eds., Elsevier, New York, pp. 191–260.
Keefe D. L., Earnest D. J., Nelson D., Takahashi J., and Turek F. W. (1987) A cholinergic antagonist, mecamylamine, blocks the phase-shifting effects of light on the circadian rhythm of locomotor activity in the golden hamster.Brain Res. 403; 308–312.
Kehoe J., Sealock R., and Bon C. (1976) Effects of α toxins from bungarus multicinctus and bungarus caeruleus on cholinergic responses in Aplysia neurones.Brain Res. 10; 527–540.
Kemp G., Bentley L., McNamee M., and Morley B. (1985) Purification and characterization of the αbungarotoxin binding protein from rat brain.Brain Res. 347; 274–283.
Kemp G. and Morley B. J. (1986) Ganglionic AChRs and high affinity nicotinic binding sites are not equivalent.FEBS Letts. 205; 265–268.
Keyser K., Hughes T., Whiting P., Lindstrom J., and Korten H. (in preparation) Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptor.
Kistler J., Stroud R., Klymkowsky M., Lalancette R., and Fairclough R. (1982) Structure and function of an acetylcholine receptor.Biophys. J. 37; 371–383.
Kley N., Loeffler J-P., Pittius C. W., Hollt V. (1987) Involvement of ion channels in the induction of proenkephalin A gene expression by nicotine and cAMP in bovine chromaffin cells.J. Biol. Chem. 262; 4083–4089.
Klymkowksy M., Neuser J., and Stroud R. (1980) Protease effects on the structure of acetylcholine receptor membranes fromTorpedo californica.J. Cell Biol. 8; 823–838.
Kordossi A. and S. Tzartos (1987) Conformation of cytoplasmic segments of acetylcholine receptor α and β subunits by monoclonal antibodies: sensitivity of the antibody competition approach.EMBO J. 6; 1605–1610.
Kouvelas E. D., Dichter M. A., (1987) Sympathetic neurons develop receptors for αbungarotoxin in vitro, but toxin does not block nicotinic receptors.Brain Res. 154; 83–93.
Kubalek E., Ralston S., and Lindstrom J. (1987) Location of subunits within the acetylcholine receptor: analysis of tubular crystals fromTorpedo marmorata.J. Cell Biol. 105; 9–18.
Kubo T., Maeda A., Sugimoto K., Akiba I., Mikami A., Takahashi H., Haga T., Haga K., Ichiyama A., Kangawa K., Matsuo H., Hirose T., and Numa S. (1986) Primary structure of porcine cardiac muscarinic acetylcholine receptor deduced from the cDNA sequence.FEBS Letts. 209; 367–373.
Kubo T., Noda M., Takai T., Tanabe T., Kayano T., Shimizu S., Tanaka K., Takahashi H., Hirose T., Inayama S., Kikuno R., Miyata T., and Numa S. (1985) Primary structure of δ subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence.Eur. J. Biochem. 149; 5–13.
Kurosaki T., Fukuda K., Kouno T., Mori Y., Tanaka K., Mishina M., and Numa S. (1987) Functional properties of nicotinic acetylcholine receptor subunits expressed in various combinations.FEBS Letts. 214; 253–258.
Kyte J. and Doolittle R. (1982) A simple method for displaying the hydropathic character of a protein.J. Mol. Biol. 157; 105–132.
Langdon R. B. and Freeman J. A. (1987) Pharmacology of retinotectal transmission in the goldfish: effects of nicotinic ligands, strychnine, and kynurenic acid.J. Neurosci. 7; 760–773.
LaPolla R. J., Mayne K. M., and Davidson N. (1984) Isolation and characterization of a cDNA clone for the complete protein coding region of the δ subunit of the mouse acetylcholine receptor.PNAS USA 81; 7970–7974.
La Rochelle W., Wray B., Sealock R., and Froehner S. (1985) Immunochemical demonstration that amino acids 360–377 of the acetylcholine receptor δ subunit are cytoplasmic.J. Cell Biol. 100; 684–691.
Laufer R. and J.-P. Changeux (1987) Calcitonin gene-related peptide elevates cyclic AMP Levels in chick skeletal muscle: possible neurotrophic role for a coexisting neuronal messenger.EMBO J. 6; 901–906.
Leprince P. (1983) Chemical modification of the nicotinic cholinergic receptor of PC-12 nerve cell.Biochem. 22; 5551–5556.
Leprince P. (1986) Studies on the nicotinic cholinergic receptor of sympathetic neurones. Nicotinic Acetylcholine Receptor, Maelicke A., ed., NATO ASI Series H, vol. 3, Springer-Verlag, Heidelberg., pp. 333–344.
Lindstrom J. (1985) Immunobiology of myasthenia gravis, experimental autoimmune myasthenia gravis, and Lambert-Eaton syndrome.Ann. Rev. Immunol. 3; 109–131.
Lindstrom J., Campbell M., and Nave B. (1978) Specificities of antibodies to acetylcholine receptors.Muscle Nerve 1; 140–145.
Lindstrom J., Criado M., Hochschwender S., Fox J. L., and Sarin V. (1984) Immunochemical tests of acetylcholine receptor subunit models.Nature 311; 573–575.
Lindstrom J., Criado M., Ratnam M., Whiting P., Ralston S., Rivier J., Sarin V., and Sargent P. (1987) Using monoclonal antibodies to determine the structures of acetylcholine receptors from electric organs, muscles, and neurons. Ann, NYAcad, Sci.
Lindstrom J., Gullick W., Conti-Tronconi B., and Ellisman M. (1980) Proteolytic nicking of the acetylcholine receptor.Biochemistry 19; 4791–4795.
Lindstrom J., Merlie J., and Yogeeswaran G. (1979) Biochemical properties of acetylcholine receptor subunits fromTorpedo californica.Biochemistry 18; 4465–4470.
Lindstrom J., Seybold M., Lennon V., Whittingham S., and Duane D. (1976) Antibody to acetylcholine receptor in myasthenia gravis: prevalence, clinical correlates, and diagnostic value.Neurology 26; 1054–1059.
Lindstrom J., Tzartos S., Gullick W., Hochschwender S., Swanson L., Sargent P., Jacob M., and Montal M. (1983) Use of monoclonal antibodies to study acetylcholine receptor from electric organs, muscle, and brain and the autoimmune response to receptor in myasthenia gravis. Cold Spring Harbor Symposia on Quant. Biol. XLVIII; 89–99.
Lippiello P. M. and Fernandes K. G. (1986) The binding of L-[3H]nicotine to a single class of high affinity sites in rat brain membranes.Mol. Pharmacol. 29; 448–454.
Lippiello P. M., Sears S. B. and Fernandes K. G. (1987) Kinetics and mechanism of L-[3H] nicotine binding to putative high affinity receptor sites in rat brain.Mol. Pharmacol. 31; 392–400.
Lipton S. A., Aizenman E., and Loring R. (1987) Neural nicotinic responses in solitary mammalian retinal ganglion cells.Pflugers Arch. 410: 37–43
Lomo T. and Rosenthal J. (1972) Control of ACh sensitivity by muscle activity in the rat.J. Physiol. 221; 493–513.
London E. and Connolly R. (1985) Distribution of cerebral metabolic effects of nicotine in the rat.Eur. J. Pharmac. 110; 391–392.
London E. D., Waller S. B., and Wamsley J. K. (1985) Autoradiographic localization of [3H] nicotine binding sites in rat brain.Neurosci. Lett. 53; 179–184.
Loring R. H. and Zigmond R. E. (1987) Ultrastructural distribution of [125I]Toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors.J. Neurosci. 7; 2153–2162.
Loring R. H., Andrews D., Lane W., and Zigmond R. E. (1986) Amino acid sequence of toxin F, a snake venom toxin that blocks neuronal nicotinic receptors.Brain Res. 38; 30–37.
Loring R. H., Dahm L. M., and Zigmond R. E. (1985) Localization of αbungarotoxin binding sites in the ciliary ganglion of the embryonic chick: an autoradiographic study of the light and electron microscopic level.Neurosci. 14; 645–660.
Loring R. H., Chiappinelli V. A., Zigmond R. E., and Bohen J. B. (1984) Characterization of a snake venom neurotoxin which blocks nicotinic transmission in the avian ciliary ganglion.Neurosci. 11; 989–999.
Lubbert H., Hoffman B. J., Snutch T. P., Van Dyke T., Levine A. J., Hartig P., Lester H., and Davidson N. (1987) cDNA cloning of a serotonin 5-HT 1C receptor by electrophysiological assays of mRNA-injectedXenopus oocytes.PNAS USA 84; 4332–4336.
Lukas R. J. (1986) Immunochemical and pharmacological distinctions between curaremimetic neurotoxin binding sites of central, autonomic, and peripheral origin.PNAS USA 83; 5741–5745.
Lukas R. J. and Bennet E. L. (1980) Chemical modification and reactivity of sulfhydryls and disulfides of rat brain nicotinic-like acetylcholine receptors.J. Biol. Chem. 255; 5573–5577.
Mamalaki C., Stephenson A., and Barnard E. (1987) The GABA/benzodiazepine receptor is a heterotetramer of homologous α and β subunits.EMBO 6; 561–565.
Mansour N. A., Eldefrawi M. E., and Eldefrawi A. T. (1977) Isolation of putative acetylcholine receptor proteins from housefly brain.Biochem. 16; 4126–4132.
Marks M. J. and A. C. Collins (1982) Characterization of nicotine binding in mouse brain and comparison with binding of αbungarotoxin and quinuclidinly benzilate.Mol. Pharmacol. 22; 554–564.
Marshall L. M. (1981) Synaptic localization of αbungarotoxin binding which blocks nicotinic transmission at from sympathetic neurons.PNAS USA 78; 1948–1952.
Martino-Barrows A. M. and Kellar K. J. (1987)3[H] acetylcholine and3H(-)nicotine label the same recognition site in rat brain.Molec. Pharm 31; 169–174.
McCormick D. A. and D. A. Prince (1987) Acetylcholine causes rapid nicotinic excitation in the medial habenular nucleus of guinea pig, in vitro.J. Neurosci. 7; 742–752.
Meeker R. B., Michels K. M., Libber M. T., and Hayward J. N. (1986) Characteristics and distribution of high and low affinity αbungarotoxin binding sites in rat hypothalamus.J. Neurosci. 6; 1866–1875.
Mehraban F., Kemshead J. T., and Dolly J. O. (1984) Properties of monoclonal antibodies to nicotinic acetylcholine receptor from chick muscle.Eur. J. Biochem. 138; 53–61.
Merlie J. P., Isenberg K., Russell S., and Sanes J. (1984) Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe.J. Cell Biol. 99; 325–332.
Merlie J. P., Lindstrom J. (1983) Assembly in vivo of mouse muscle acetylcholine receptor: identification of an α subunit species which may be an assembly intermediate.Cell 34; 747–757.
Merlie J., Sebbane R., Gardner S., Olson E., and Lindstrom J. (1983a) The regulation of acetylcholine receptor expression in mammalian musCold Spring Harbor Symposia on Quant. Biol. XLVII; 135–146.
Merlie J., Sebbane R., Gardner S., Olson E., and Lindstrom J. (1983b) Regulation of acetylcholine receptor gene expression: molecular cloning of a cDNA specific for α subunit of the receptor from the mouse muscle cell line BC3H1.PNAS USA 80; 3845–3849.
Merlie J., Sebbane R., Gardner S., Olson E., and Lindstrom J. (1983c) cDNA clone for the α subunit of the acetylcholine receptor form the mouse muscle cell line BC3H-1.PNAS USA 80; 3845–3849.
Messing A. and Kim S. U. (1981) Development of αbungarotoxin receptors in cultured chick ciliary ganglion neurons.Brain Res. 208; 479–486.
Metcalf R. (1948) The mode of action of organic insecticides.National Research Council Rev. No. 1, pp. 1–84.
Meledi R. and A. C. Szczepaniak (1981) Effect of Dendroaspis neurotoxins on synaptic transmission in the spinal chord of the frog. Proc. R. Soc. (London). B190; 267–274.
Mills A., and Wonnacott S. (1984) Antibodies to nicotinic acetylcholine receptors used to probe the structural and functional relationships between brain αbungarotoxin binding sites and nicotinic receptors.Neurochem. Intl. 6; 249–257.
Mishina M., Kurosaki T., Tobimatsu T., Morimoto Y., Noda M., Yamamoto T., Terao M., Lindstrom J., Takahashi T., Kuno M., and Numa S. (1984) Expression of functional acetylcholine receptor from cloned cDNAs. Nature 307; 604–608.
Mishina M., Tobimatsu T., Imoto K., Tanaka K., Fujita Y., Fukuda K., Kurasaki M., Takahashi H., Morimoto Y., Hirose T., Inayama S., Takahashi H., Kuno M., and Numa S. (1985) Location of functional regions of acetylcholine receptor α subunit by site-directed mutagenesis.Nature 313; 364–369.
Mishina M., Takae T., Imoto K., Noda K., Takahashi T., Numa S., Methfessel C., and Sakmann B. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor.Nature 321; 406–411.
Morley B. J. and Kemp G. E. (1981) Characterization of a putative nicotinic acetylcholine receptor in mammalian brain.Brain Res. Rev. 3; 81–104.
Morley B. J., Dwyer D. S., Strang-Brown P. F., Bradley R. J., and Kemp G. E. (1983) Evidence that certain peripheral anti-acetylcholine receptor antibodies do not interact with brain αBgt binding sites.Brain Res. 262; 109–116.
Nef P., Mauron A., Romaine S., Alliod C., and Ballivet M., (1984) Structure, linkage, and sequence of the two genes encoding the κ and γ subunits of the nicotinic acetylholine receptor.PNAS USA 81; 7975–7979.
Nef P., C. Oneyser, T. Barkas, and M. Balliver (1986) Acetylcholine receptor related genes expressed in the nervous system.Nicotinic Acetylcholine Receptor, Maelicke A., ed., NATO ASEI Series H, vol. 3, Springer-Verlag, Heidelberg., pp. 417–422.
Neumann D., Gershoni J., Fridkin M., and Fuchs S. (1985) Antibodies to synthetic peptides as probes for the binding site on the α subunit of the acetylcholine receptor.PNAS USA 82; 9250–9253.
Noda M., Takahashi M., Tanabe T., Toyosato M., Kikyotani S., Tadaski H., Asai M., Takashima H., Inayama S., Takashi M., and Numa S. (1983b) Primary structures of β- and δ-subunit precursors ofTorpedo californica acetylcholine receptor deduced from cDNA sequences.Nature 301; 251–255.
Nomoto H., Takahashi N., Nagaki Y., Endo S., Arata Y., and Hayashi K. (1986) Carbohydrate structures of acetylcholine receptor fromTorpedo californica and distribution of oligosaccharides among the subunit.Eur. J. Biochem. 157; 233–242.
Norman R., Mehraban R., Barnard E. A., and Dolly J. O. (1982) Nicotinic acetylcholine receptor from chick optic lobe.PNAS USA 79; 1321–1325.
Olsen R. W. (1985) The γ-aminobutyric acid/benzodiazipine/barbiturate receptor-chloride ion channel complex of mammalian brain.New Insights Into Synaptic function, Edelman G. M., Gall W. E., and Cowan W. M., eds., Neurosciences Research Foundation, Wiley, New York.
Olson E., Glaser L., and Merlie J. (1984) α and β subunits of the nicotinic acetylcholine receptor contain covalently bound lipid.J. Biol. Chem. 259; 5364–5367.
Ono J. K. and Salvaterra P. M. (1981) Snake α toxin effects on cholinergic and non-cholinergic responses ofAplysia californica.J. Neurosci. 1; 259–270.
Oswald R. E. and Freeman J. A. (1979) Ligand responses of αbungarotoxin binding sites for skeletal muscle and optic lobe of the chick.J. Biol. Chem. 253; 8507–8512.
Oswald R. E. and Freeman J. A. (1981) αBungarotoxin binding and central nervous system nicotinic acetylcholine receptors.Neurosci. 6; 1–14.
Oswald R. E., Pennow N., and McLaughlin J., (1985) Demonstration and affinity labeling of a stereo selective binding site for a benzomorphan opiate on acetylcholine receptor-rich membranes fromTorpedo electroplaque.PNAS USA 82; 940–944.
Patrick J. and Lindstrom J. (1973) Autoimmune response to acetylcholine receptor.Science 180; 871–872.
Patrick J. and Stallcup W. B. (1977a) Immunological distinction between acetylcholine receptor and the αbungarotoxin binding component on sympathetic neurons.PNAS USA 76; 4689–4692.
Patrick J. and Stallcup W. B. (1977b) αBungarotoxin binding and cholinergic receptor function on a rat sympathetic cell line.J. Biol. Chem. 252; 8629–8633.
Pazdernik T., Cross R., Mewes K., Samson F., and Nelson S. (1982) Superior colliculus activation by retinal nicotinic ganglion cells: a 2-deoxyglucose study.Brain Res. 234; 197–200.
Perry E., Perry R., Smith C., Dick D., Candy J., Edwardson J., Fairbairn A., and Blessed G. (1987) Nicotinic receptor abnormalities in Alzheimer’s and Parkinson’s diseases.J. Neurol. Neurosurg. Psych. 50; 806–809.
Popot J.-L. and Changeux J.-P. (1984) Nicotinic receptor of acetylcholine: structure of an oligomeric membrane protein.Physiol. Rev. 64; 1162–1239.
Quik M., and Lamarca M. V. (1982) Blockade of transmission in rat sympathetic ganglia by a toxin which copurifies with αbungarotoxin.Brain Res. 238; 385–399.
Quik M., Geertsen S., and Trifaro J. M. (1987) Marked up regulation of the αbungarotoxin site in adrenal chromaffin cells by specific nicotinic antagonists.Molec. Pharm. 31; 385–391.
Radeke M. J., Misko T. P., Hsu C., Herzenberg L. A., and Shooter E. M. (1987) Gene transfer and molecular cloning of the rat nerve growth factor receptor.Nature 325; 593–597.
Raftery M., Hunkapillar M., Strader C., and Hood L. (1980) Acetylcholine receptor: complex of homologous subunits.Science 208; 1454–1457.
Ralston S., Sarin V., Thanh H., Rivier J., Fox J. L., and Lindstrom J. (1987) Synthetic peptides used to locate the αbungarotoxin binding site and immunogenic regions on a subunits of the nicotinic acetylcholine receptor.Biochemistry 26; 3261–3266.
Rapier C., Harrison R., Lunt G. G., and Wonnacott S. (1985) Neosurugatoxin blocks nicotinic acetylcholine receptors in the brain.Neurochem Intl. 7; 389–396.
Rapier C., Wonnacott S., Lunt G., and Albuquerque E. X. (1987) The neurotoxin histrionicotoxin interacts with the putative ion channel of the nicotinic acetylcholine receptors in the central nervous system.FEBS Letts. 212; 292–296.
Ratnam M. and Lindstrom (1984) Structural features of the nicotinic acetylcholine receptor revealed by antibodies to synthetic peptides.BBRC 122; 1225–1233.
Ratnam M., Sargent P. B., Sarin V., Fox J. L., Le Nguyen D., Rivier J., Criado M., and Lindstrom J. (1986a) Location of antigenic determinants on primary sequences of subunits of nicotinic acetylcholine receptor by peptide mapping.Biochemistry 25; 2621–2632.
Ratnam M., Le Nguyen D., Rivier J., Sargent P. B., and Lindstrom J. (1986b) Transmembrane topography of nicotinic acetylcholine receptor: immunochemical tests contradict theoretical predictions based on hydrophobicity profiles.Biochemistry 25; 2633–2643.
Ratnam M., Gullick W., Spiess J., Wan K., Criado M., and Lindstrom J. (1986c) Structural heterogeneity of the α subunits of the nicotinic acetylcholine receptor in relation to agonist affinity alkylation and antagonist binding.Biochem 25; 4268–4275.
Ravdin P. M. and Berg D. K. (1979) Inhibition of neuronal acetylcholine sensitivity by a toxin fromBungarus multicintus venom.PNAS USA 75; 2072–2076.
Reiner A. (1987) A VIP-like peptide co-occurs with substance P and enkephalin in cholinergic preganglionic terminals of the avian ciliary ganglion.Neurosci. Letts. 78; 22–28.
Reynolds J. and Karlin A., (1978) Molecular weight in detergent solution of acetylcholine receptor fromTorpedo californica.Biochemistry 17; 2035–2038.
Romano C. and Goldstein A. (1980) Stereospecific nicotine receptors in rat brain membranes.Science 210; 647–649.
Safran A., Neumann D., and Fuchs S. (1986) Analysis of acetylcholine receptor phosphorylation sites using antibodies to synthetic peptides and monoclonal antibodies.EMBO J. 5; 3175–3176.
Saiani L., Kageyama H., Conti-Tronconi B. M., and Guidotti A. (1985) Purification and characterization of a bungarotoxin polypeptide which blocks nicotinic receptor function in primary culture of adrenal chromaffin cells.Molec. Pharmacol. 25; 327–336.
Sakmann B., Methfessel C., Mishina M., Takahashi T. Takai T., Kurasaki M., Fukuda K., and Numa S. (1985) Role of acetylcholine receptor subunits in gating of the channel.Nature 318; 538–543.
Salpeter M. and Harris M. (1983) Distribution and turnover rate of acetylcholine receptors throughout the junction folds at a vertebrate neuromuscular junction.J. Cell Biol. 96; 1781–1785.
Sargent P., Hedges B., Tsavaler L., Clemmons L., Tzartos S., and Lindstrom J. (1983) The structure and transmembrane nature of the acetylcholine receptor in amphibian skeletal muscles revealed by crosseeacting monoclonal antibodies.J. Cell Biol. 98; 609–618.
Sargent P., Pike S., Nadel D., Lindstrom J. (in preparation) Nicotinic acetylcholine receptor-like molecules in the optic tectum are extrasynaptic and associated with retinal afferents.
Sattelle D. B., Harrow I. D., Hu B., Pelhate M., Gepner J. I., and Hall L. M. (1983) αbungarotoxin blocks excitatory synaptic transmission between circal sensory neurones and giant interneurone two of the cockroach,Periplaneta americana.J. Exptl. Biol. 107; 473–489.
Schleiffer L. S., and Eldefrawi M. E. (1974) Identification of the nicotinic and muscarinic acetylcholine receptors in subcellular fractions of mouse brains.Neuropharmacol. 13; 53–63.
Schneider M., Adee C., Betz H., and Schmidt J. (1985) Biochemical characterization of two nicotinic receptors from the optic lobe of the chick. J.Biol. Chem. 260; 14505–14512.
Schoepfer R., Luther M., and Lindstrom J. (1988) The human medulloblastoma cell line TE671 expresses a muscle-like acetylcholine receptor: cloning of the a subunit cDNA.FEBS Lett., in press.
Schofield P., Darlison M., Fujita N., Burt D., Stephenson F., Rodriquez H., Rhee L., Ramachandran J., Reale V., Glencorse T. Seeburg P., and Barnard E. (1987) Sequence and functional expression of the GABAA receptor shows a ligand-gated receptor superfamily.Nature 328; 221–227.
Schwartz R.D., McGee R., and Kellar K.J. (1982) Nicotinic cholinergic receptors labeled by [3H] acetylcholine in rat brain.Mol. Pharmacol. 22; 56–62.
Sealock R., Wray B., and Froehner S. (1984) Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor inTorpedo postsynaptic membranes using monoclonal antibodies.J. Cell Biol. 98; 2239–2244.
Sebbane R., Clokey G., Merlie J. P., Tzartos S., and Lindstrom J. (1983) Characterization of the mRNA for mouse muscle acetylcholine receptor α subunit by quantitative translation in vitro.J. Biol. Chem. 258(5); 3294–3303.
Shershen H., Reith M., Hashim A., and Lajtha A. (1984) Endogenous material in brain inhibiting [3H]nicotine and [3H]acetylcholine binding.J. Neurosci. Res. 12; 563–569.
Seto A., Arimatsu Y., and Amano T. (1981) Subunit structure of αbungarotoxin binding component in mouse brain.J. Neurochem. 37; 210–216.
Shibahara S., Kubo T., Perski H. J., Takahashi H., Noda M., and Numa S. (1985) Cloning and sequence analysis of human genomic DNA encoding δ subunit precursor of muscle acetylcholine receptor.Eur. J. Biochem. 146; 15–22.
Shimohama S., Taniguchi T., Fujiware M., and Kameyama M. (1985) Biochemical characterization of the nicotinic cholinergic receptors in the human brain: binding of (−) [3H]nicotine.J. Neurochem. 45; 604–610.
Shimohama S., Taniguchi T., Fujiwara M., and Kameyama (1986) Changes in nicotinic and muscarinic cholinergic receptor in Alzheimer type dementia.J. Neurochem. 46; 288–293.
Smith M., Stollberg J., Berg D. K., and Lindstrom J. (1985) Characterization of a component in chick ciliary ganglia that crossreacts with monoclonal antibodies to muscle and electric organ acetylcholine receptor.J. Neurosci. 5; 2726–2731.
Smith M., Margiotta J., Franco A., Lindstrom J., and Berg D. (1986) Cholinergic modulation of an ace-tylcholine receptor-like antigen on the surface of chick ciliary ganglion neurons in cell culture.J. Neurosci. 6; 946–953.
Smith M., Merlie J., and Lawrence J. (1987) Regulation of phosphorylation of nicotinic acetylcholine receptors in mouse BC3H1 myocytes.PNAS USA 84; 6601–6605.
Sorenson E. M., Culver P., and Chiappinelli V. A. (1987) Lophotoxin: selective blockade of nicotinic transmission in autonomic ganglia by a coral neurotoxin.Neurosci. 20; 875–884.
Souroujon M., Neumann D., Pizzighella S., Safran A., and Fuchs S. (1986) Localization of a highly immunogenic region on the acetylcholine receptor a subunit.BBRC 135; 82–89.
Stollberg J. and Berg D. (1987) Neuronal acetylcholine receptors: fate of surface and internal pools in cell culture.J. Neurosci,7; 1809–1815.
Stollberg J., Whiting P. J., Lindstrom J. M., and Berg D. K. (1986) Functional blockade of neuronal acetylcholine receptors by antisera to a putative receptor from brain.Brain Res. 378; 179–182.
Strader C., Sigal I., Register R., Candelore M., Rands E., and Dixon R. (1987) Identification of residues required for ligand binding to the β adrenergic receptor.PNAS USA 84; 4384–4388.
Sugiyama H. and Yamashita Y. (1986) Characterization of putative nicotinic acetylcholine receptors solubilized from rat brains.Brain Res. 373; 22–26.
Sumikawa K., Houghton M., Emtage J. S., Richards B. M., and Barnard E. A. (1981) Active multi-subunit ACh receptor assembled by translation of heterologous mRNA inXenopus oocytes.Nature 292; 862–864.
Swanson K. K., Allen C. N., Aronstam R. S., Rapaport, H., and Albuquerque E. X. (1986) Molecular mechanisms of the potent and sterospecific nicotinic receptor agonist (+) Anatoxin-a.Mol. Pharmacol. 29; 250–257.
Swanson L., Lindstrom J., Tzartos S., Schmued L., O’Leary D., and Cowan W. (1983) Immunohistochemical localization of monoclonal antibodies to the nicotinic acetylcholine receptor in the midbrain of the chick.PNAS USA 80; 4532–4536.
Swanson L., Simmons D., Whiting P., and Lindstrom J. (1987) Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system.J. Neurosci. 7; 3334–3342.
Syapin P., Salvaterra P., and Engelhardt J. (1982) Neuronal-like features of TE671 cells: presence of a functioning nicotinic cholinergic receptor.Brain Res. 231; 365–377.
Takai T., Noda M., Furutani Y., Takahashi H., Notake M., Shimizu S., Kayano T., Tanabe T., Tanaka K., Hirose T., Inayama S., and Numa S. (1984) Primary structure of γ subunit precursor of calf-muscle acetylcholine receptor deduced from the cDNA sequence.Eur. J. Biochem. 143; 109–115.
Takai T., Noda M., Mishina M., Shimizu S., Furutani T., Kayano T., Ikeda T., Kubo T., Takahashi H., Takahashi T., Kuno M., and Numa S. (1985) Cloning sequencing and expression of cDNA for a novel subunit of acetylcholine receptor from calf muscle.Nature 315; 761–764.
Tanabe T., Noda M., Furutani Y., Takai T., Takahashi H., Tanaka K., Hirose T., Inayama S., and Numa S. (1984) Primary structure of β subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence.Eur. J. Biochem. 144; 11–17.
Tanabe T., Takeshima H., Mikomi A., Flockerzi V., Takahashi H., Kangowa K., Kojima M., Matsuo H., Hirose T., and Numa S. (1987) Primary structure of the receptor for calcium blockers from skeletal muscle.Nature 328; 313–318.
Tas P., Dress H., and Koschel (1987) General anesthetics can competitively interfere with sensitive membrane proteins.PNAS USA 84; 5972–5975.
Tempel B., Papozian D., Schwartz T., Jan Y., and Jan L. (1987) Sequence of a probable potassium channel component encoded at Shaker locus ofDrosophila.Science 237; 770–775.
Tobimatsu T., Fujita Y., Fukuda K., Tanaka K., Mori Y., Konno T., Mishina M., and Numa S. (1987) Effects of substitution of putative transmembrane segments on nicotinic acetylcholine receptor function.FEBS Lett. 222 56–62.
Tzartos S., Hochschwender S., Vasquez P., and Lindstrom J. (1987) Passive transfer of experimental autoimmune myasthenia gravis by monoclonal antibodies to the main immunogenic region of the acetylcholine receptor.J. Neuroimmunol. 15; 185–194.
Tzartos S., Rand D., Einarson B., and Lindstrom J. (1981) Mapping of surface structures on electrophorus acetylcholine receptor using monoclonal antibodies.J. Biol. Chem. 256; 8635–8645.
Tzartos S., Seybold M., and Lindstrom J. (1982) Specificity of antibodies to acetylcholine receptors in sera from myasthenia gravis patients measured by monoclonal antibodies.PNAS USA 79; 188–192.
Tzartos S., Langeberg L., Hochschwender S., and Lindstrom J. (1983) Demonstration of a main immunogenic region on acetylcholine receptors from human muscle using monoclonal antibodies to human receptor.FEBS Letts. 158; 116–118.
Ullrich A., Bell J., Chen E., Herrva R., Petruzelli L., Dull T., Gray A., Coussins L., Kiao Y., Tsubokawa M., Mason A., Seeburg P., Krunfeld C., Rosen D., and Ramachandran J. (1985) Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes.Nature 313; 756–761.
Wan K. and Lindstrom J. (1985) Effects of monoclonal antibodies on the function of acetylcholine receptors purified fromTorpedo californica and reconstituted into vesicles.Biochemistry 24; 1212–1221.
Wang G., Molinaro S., and Schmidt J. (1978) Ligand responses of αbungarotoxin binding sites from skeletal muscle and optic lobe of the chick.J. Biol. Chem. 253; 8507–8512.
Watson J., Adkins-Regan E., Whiting P., Lindstrom J., and Podleski T. (in preparation) Autoradiographic determination of the distribution of nicotinic acetylcholine receptors in the zebra finch brain.
Weinberger C., Hollenberg S., Ong E. S., Brower S., Cidlowski J., Thompson E. B., Rosenfeld M. G., and Evans R. M. (1985) Identification of human glucocorticoid receptor complementary DNA clones by epitope selections.Science 228; 740–742.
Whiting P., Cooper J., and Lindstrom J. (1978c) Antibodies in sera from patients with myasthenia gravis do not bind to acetylcholine receptors from human brain.J. Neuroimmunol. 16; 205–213.
Whiting P., Esch F., Shimasaki S., and Lindstrom J. (1987b) Neuronal nicotinic acetylcholine receptor β subunit is coded for by the cDNA clone α4.FEBS Letts. 219; 459–463.
Whiting P. and Lindstrom J. (1986a) Purification and characterization of a nicotinic acetylcholine receptor from chick brain.Biochem. 25; 2082–2093.
Whiting P. and Lindstrom J. (1986b) Pharmacological properties of immunoisolated neuronal nicotinic receptors.J. Neurosci. 6; 3061–3069.
Whiting P. and Lindstrom J. (1987a) Affinity labeling of neuronal acetylcholine receptors localizes the neurotransmitter binding site to the β subunit.FEBS Letts. 213; 55–60.
Whiting P. and Lindstrom J. (1987b) Purification and characterization of a nicotinic acetylcholine receptor from rat brain.PNAS USA 84; 595–599.
Whiting P and Lindstrom J. (1988) Characterization of bovine and human neuronal nicotinic acetylcholine receptros using monoclonal ntibodies.J. Neuroscience (in press).
Whiting P., Liu R., Morley B., and Lindstrom J. (1987d) Structurally different neuronal nicotinic acetylcholine receptor subtypes purified and characterized using monoclonal antibodies.J. Neuroscience.
Whiting P., Schoepfer R., Swanson L., Simmons D., and Lindstrom J. (1987a) A monoclonal antibody to nicotinic receptors from brain identified a functional neuronal acetylcholine receptor of PC12 cells.Nature 317; 515–518.
Wolosin J. M., Lyddiatt A., Dolly J. O., and Barnard E. A. (1980) Stoichiometry of the ligand binding sites in the acetylcholine receptor oligomer from muscle and from electric organ.Eur. J. Biochem. 109; 495–505.
Wong G. K. and Schmidt J. (1976) Receptors for αbungarotoxin in the developing visual system of the chick.Brain Res. 114; 524–529.
Wong G. K., Molinaro S., and Schmidt J. (1978) Ligand responses of αbungarotoxin binding sites from skeletal muscle and optic lobe of the chick.J. Biol. Chem. 253; 8507–8512.
Wonnacott S. Brain nicotine binding sites.Human Toxicology.6; 343–353.
Wonnacott S. (1986) αBungarotoxin binds to low affinity nicotine binding sites in rat brain.J. Neurochem. 47; 1706–1712.
Wonnacott S., Fryer L., and Lunt G. G. (1987) Nicotine-evoked [3H]GABA release from hippocampal synaptosomes.J. Neurochem. 48 Suppl.; S72.
Wonnacott S., Harrison R., and Lunt G. (1982) Immunological crossreactivity between the αbungarotoxin-binding component from rat brain and nicotinic acetylcholine receptor.J. Neuroimmunol. 3; 1–13.
Yamada S., Isogai M., Kagawa Y., Tokayanagi N., Hayashi E., Tsujiki K., and Kosuge T. (1985) Brain nicotinic acetylcholine receptors: biochemical characterization by neosurugatoxin.Molec. Pharmacol. 28; 120–127.
Yamada S., Kagawa Y., Ushijima H., Takayanagi N., Tomita T., and Hayashi E. (1987) Brain nicotinic cholinoceptor binding in spontaneous hypertension.Brain Res. 410; 212–218.
Yoshida K., Kato Y., and Imura H. (1980) Nicotine-induced release of noradrenaline from hypothalamic synaptosomes.Brain Res. 182; 361–368.
Young E., Ralston E., Blake J., Ramachandran J., Hall Z., and Stroud R. (1985) Topological mapping of acetylcholine receptor: evidence for a model with five transmembrane segments and a cytoplasmic COOH-terminal peptide.PNAS USA 82; 626–630.
Yu L., LaPolla R. J., and Davidson N. (1986) Mouse muscle nicotinic acetylcholine receptor γ subunit: cDNA sequence and gene expression.Nucleic Acids Res. 14; 3539–3555.
Zhang X., Stjernlof P., Adem A., and Nordberg A. (1987) Anatoxin-a, a potent ligand for nicotinic cholinergic receptors in rat brain.Eur. J. Pharmac. 135; 457–458.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lindstrom, J., Schoepfer, R. & Whiting, P. Molecular studies of the neuronal nicotinic acetylcholine receptor family. Mol Neurobiol 1, 281–337 (1987). https://doi.org/10.1007/BF02935740
Issue Date:
DOI: https://doi.org/10.1007/BF02935740