The molecular biology of neuronal nicotinic acetylcholine receptors

Critical Reviews in Toxicology

Volumn 27, Issue 3, 1997, Pages 299-318

  Boyd, R Thomas ^a,b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Ion channels; Pharmacology; Regulation; Subtype diversity

Indexed keywords

ION CHANNEL; NICOTINIC RECEPTOR; RECEPTOR SUBTYPE;

BRAIN; GANGLION; HUMAN; MOLECULAR BIOLOGY; MOLECULAR CLONING; NERVE CELL; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN PURIFICATION; RECEPTOR GENE; RETINA; REVIEW;

EID: 0030980834     PISSN: 10408444     EISSN: None     Source Type: Journal    
DOI: 10.3109/10408449709089897     Document Type: Review

References (163)

1. Amar, M., Thomas, P., Johnson, C. et al., Agonist pharmacology of the neuronal al nicotinic receptor expressed in Xenopus oocytes, FEBS Lett., 327, 284, 1993.
2. Anand, R., Conroy, W. G., Schoepfer, R. et al., Neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes have a pentameric quaternary structure. J. Biol. Chem., 266, 11192, 1991.
3. Anand, R., Peng, X., and Lindstrom, J., Homomeric and native α7 acetylcholine receptors exhibit remarkably similar but non-identical pharmacological properties, suggesting that the native receptor is a heteromeric protein complex, FEBS Lett., 327, 241, 1993a.
4. Anand, R., Peng, X., Ballesta, J. J. et al., Pharmacological characterization of α-bungarotoxin-sensitive acetylcholine receptors immunoisolated from chick retina: contrasting properties of α7 and α8 subunit-containing subtypes, Mol. Pharm., 44, 1046, 1993b.
5. Arenella, L. S., Oliva, J. M., and Jacob, M. H., Reduced levels of acetylcholine receptor expression in chick ciliary ganglion neurons developing in the absence of innervation, J. Neurosci., 13, 4525, 1993.
6. Ballivet, M., Nef, P., Couturier, S. et al., Electrophysiology of a chick neuronal nicotinic acetylcholine receptor expressed in Xenopus oocytes after cDNA injection, Neuron, 1, 847, 1988.
7. Betrand, D., Ballivet, M., and Rungger, D., Activation and blocking of neuronal nicotinic acetylcholine receptor reconstituted in Xenopus oocytes, Proc. Natl. Acad. Sci. U.S.A., 87, 1993, 1990.
8. Bertrand, D., Bertrand, S., and Ballivet, M., Pharmacological properties of the homomeric α7 receptor, Neurosci. Lett., 146, 87, 1992.
9. Bessis, A., Simon-Chazottes, D., Devillers-Thiery, A. et al., Chromosomal localization of the mouse genes coding for α2, α3, α4, and β2 subunits of neuronal nicotinic acetylcholine receptor, FEBS Lett., 264, 48, 1990.
10. Boulter, J., Evans, K., Goldman, D. et al., Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor alpha-subunit. Nature, 319, 368, 1986.
11. Boulter, J., Connolly, J., Deneris, E. et al., Functional expression of two neural nicotinic acetylcholine receptors from cDNA clones identifies a gene family, Proc. Natl. Acad. Sci. U.S.A., 84, 7763, 1987.
12. Boulter, J., O'Shea-Greenfield, A., Duvoisin, R. M. et al., α3, α5 and β4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a cluster, J. Biol. Chem., 265, 4472, 1990.
13. Boyd, R. T., Jacob, M. H., Couturier, S. et al., Expression and regulation of neuronal acetylcholine receptor mRNA in chick ciliary ganglia, Neuron, 1, 495, 1988.
14. Boyd, R. T., Jacob, M. H., McEachern, A. E. et al., Nicotinic acetylcholine receptor mRNA in dorsal root ganglion neurons, J. Neurobiol., 22, 1, 1991.
15. Britto, L. R., Keyser, K. T., Lindstrom, J. M. et al., Immunohistochemical localization of α-bungarotoxin binding proteins in the chick brain, J. Comp. Neurol., 317, 325, 1992a.
16. Britto, L. R. G., Hamassaki-Britto, D. E., Ferro, E. S. et al., Neurons of the chick brain and retina expressing both α-bungarotoxin and α-bungarotoxin-insensitive nicotinic acetylcholine receptors: an immunohistochemical analysis. Brain Res., 590, 193, 1992b.
17. Cachelin, A. B. and Jaggi, R., β subunits determine the time course of desensitization in rat α3 neuronal nicotinic acetylcholine receptors. Pflugers Arch., 419, 579, 1991.
18. Cachelin, A. B. and Rust, G., Unusual pharmacology of (+)-tubocurarine with rat neuronal nicotinic acetylcholine receptors containing β 4 subunits, Mol. Pharm., 46, 1168, 1994.
19. Chini, B., Raimond E., Elgoyhen A. B. et al., Molecular cloning and chromosomal localization of the human α7-nicotinic receptor subunit gene (CHRNA7), Genomics, 19, 379, 1994.
20. 125I]-bungarotoxin, J. Neurosci., 5, 1307, 1985.
21. Clarke, P. B. S., Recent progress in identifying nicotinic cholinoceptors in mammalian brain. Trends Pharm. Sci., 8, 32, 1987.
22. Clarke, P. B. S., The fall and rise of neuronal α-bungarotoxin binding proteins, Trends Pharm. Sci., 13, 407, 1992.
23. Clarke, P. B. S., Reuben, M., and El-Bizri, H., Blockade of nicotinic responses by physostigmine, tacrine, and other cholinesterase inhibitors in rat striatum, Br. J. Pharmacol., 111, 695, 1994.
24. Cooper, C., Couturier, S., and Ballivet, M., Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature, 350, 235, 1991.
25. Conroy, W. G., Vernallis, A., and Berg, D. K., The α5 gene product assembles with multiple acetylcholine receptor subunits to form distinctive receptor subtypes in brain, Neuron, 9, 679, 1992.
26. Conroy, W. G. and Berg, D. K., Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions, J. Biol. Chem., 270, 4424, 1995.
27. Conti-Tronconi, B. M., Dunn, S. M. J., Barnard, E. A. et al., Brain and muscle nicotinic acetylcholine receptors are different but homologous proteins, Proc. Natl. Acad. Sci U.S.A., 82, 5208, 1985.
28. Corriveau, R. and Berg, D. K., Coexpression of multiple acetylcholine receptor genes in neurons: quantification of transcripts during development, J. Neurosci., 13, 2662, 1993.
29. Corriveau, R. A. and Berg, D. K., Neurons in culture maintain acetylcholine receptor levels with far fewer transcripts than in vivo, J. Neurobiol., 25, 1579, 1994.
30. Corriveau, R. A., Romano, S. J., Conroy, W. G. et al., Expression of neuronal acetylcholine receptor genes in vertebrate skeletal muscle during development, J. Neurosci., 15, 1372, 1995.
31. Couturier, S., Bertrand, D., Matter, J.-M. et al., A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homooligomeric channel blocked by α-Btx, Neuron, 5, 847, 1990a.
32. Couturier, S., Erkman, L., Valera, S. et al., α5, α3, and non-α3: three clustered avian genes encoding neuronal nicotinic acetylcholine receptor-related subunits, J. Biol. Chem., 265, 17560, 1990a.
33. Covernton, P. J. O., Kojima, H., Sivilotti, L. G. et al., Comparison of neuronal nicotinic receptors in rat sympathetic neurones with subunit pairs expressed in Xenopus oocytes, J. Physiol., 481, 27, 1994.
34. Criado, M., Alamo, L., and Navarro, A., Primary structure of an agonist binding subunit of the nicotinic acetylcholine receptor from bovine adrenal chromaffin cells, Neurochem. Res., 17, 281, 1992.
35. Daubas, P., Devillers-Thiery, A., Geoffroy, B. et al., Differential expression of the neuronal acetylcholine receptor α2 subunit gene during chick brain development, Neuron. 5, 49, 1990.
36. Deneris, E. S., Connolly, J., Boulter, J. et al., Primary structure and expression of B2: a novel subunit of neuronal nicotinic acetylcholine receptors, Neuron, 1, 45, 1988.
37. Deneris, E. S., Boulter, J., Swanson, L. W. et al., B3: a new member of nicotinic acetylcholine receptor gene family is expressed in brain, J. Biol. Chem., 264, 6268, 1989.
38. Dineley-Miller, K. and Patrick, J., Gene transcripts for the nicotinic receptor subunit, Beta 4, are distributed in multiple areas of the rat central nervous system, Mol. Brain Res., 16, 339, 1992.
39. Dominguez del Toro, E., Juiz, J. M., Peng, X. et al., Immunocytochemical localization of the α7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system, J. Comp. Neurol., 349, 325, 1994.
40. Doucette-Stamm, L., Monteggia, L. M., Donnelly-Roberts, D. et al., Cloning and sequence of the human α7 nicotinic acetylcholine receptor, Drug Dev. Res., 30, 252, 1993.
41. Duvoisin, R. M., Deneris, E. S., Patrick, J. et al., The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: B4, Neuron, 3, 487, 1989.
42. Elgoyhen, A. B., Johnson, D. J., Boulter, J. et al., α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell, 79, 705, 1994.
43. Eng, C. M., Kozak, C. A., Beaudet, A. L. et al., Mapping of multiple subunits of the neuronal nicotinic acetylcholine receptor to chromosome 15 in man and chromosome 9 in mouse, Genomics, 9, 278, 1991.
44. Engisch, K. L. and Fischbach, G. D., The development of ACh-and GABA-activated currents in normal and target-deprived embryonic chick ciliary ganglia, Dev. Biol., 139, 417, 1990.
45. Engisch, K. L. and Fischbach, G. D., The development of ACh- and GABA-activated currents in embryonic chick ciliary ganglion neurons in the absence of innervation in vivo, J. Neurosci., 12, 1115, 1992.
46. Flores, C. M., Rogers, S. W., Pabreza, L. A. et al., A subtype of nicotinic cholinergic receptor in rat brain is comprised of α-4 and β-2 subunits and is up-regulated by chronic nicotine treatment, Mol. Pharm., 41, 31, 1992.
47. Galzi, J.-L., Revah, F., Bessis, A. et al., Functional architecture of the nicotinic acetylcholine receptor: from electric organ to brain, Ann. Rev. Pharmacol., 31, 37, 1991.
48. Galzi, J.-L. and Changeux, J.-P., Neuronal nicotinic receptors: molecular organization and regulations, Neuropharmacology, 34, 563, 1995.
49. Garcia-Guzman, M., Sala, F., Sala, S. et al., α-Bungarotoxin-sensitive nicotinic receptors on bovine chromaffin cells: molecular cloning, functional expression, and alternative splicing of the α7 subunit, Eur. J. Neurosci., 7, 647, 1995.
50. Gardette, R., Listerud, M. D., Brussard, A. B. et al., Developmental changes in transmitter sensitivity and synaptic transmission in embryonic chicken sympathetic neurons innervated in vitro, Dev. Biol., 147, 83, 1991.
51. Gerzanich, V., Anand, R., and Lindstrom, J., Homomers of α8 and α7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties, Mol. Pharm., 45, 212, 1994.
52. Goldman, D., Boulter, J., Heinemann, S. et al., Muscle denervation increases the levels of two mRNAs coding for the acetylcholine receptor α-subunit, J. Neurosci., 5, 2553, 1985.
53. Goldman, D., Simmons, D., Swanson, L. W. et al., Mapping of brain areas expressing RNA homologous to two different acetylcholine receptor α-subunit cDNAs, Proc. Natl. Acad. Sci. U.S.A., 83, 4076, 1986.
54. Goldman, D., Deneris, E. S., Luyton, W. et al., Members of a nicotinic acetylcholine receptor gene family are expressed in different regions of the mammalian central nervous system, Cell, 48, 965, 1987.
55. Goldman, D., Brenner, H. R., and Heinemann, S., Acetylcholine receptor α-, β-, γ-, and δ-subunit mRNA levels are regulated by muscle activity, Neuron, 1, 329, 1988.
56. Gotti, C., Ogando, A. E., Hanke, W. et al., Purification and characterization of an α-bungarotoxin receptor that forms a functional nicotinic channel, Proc. Natl. Acad. Sci. U.S.A., 88, 3258, 1991.
57. Grando, S. A., Horton, R. M., Pereira, E. F. et al., A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes, J. Investig. Dermatol., 105, 774, 1995.
58. Greene, L. A. and Tischler, A. S., Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor, Proc. Natl. Acad Sci. U.S.A., 73, 2424, 1976.
59. Gu, H., Wenger, B. W., Lopez, I. et al., Characterization and localization of adrenal nicotinic acetylcholine receptors: evidence that mAb35-nicotinic receptors are the principal receptors mediating adrenal catecholamine secretion, J. Neurochem., 66, 1454, 1996.
60. Gurantz, D., Harootunian, A. T., Tsien, R. Y. et al., VIP modulates neuronal nicotinic acetylcholine receptor function by a cyclic AMP-dependent mechanism, J. Neurosci., 14, 3540, 1994.
61. Hall, Z. W. and Sanes, J. R., Synaptic structure and development: the neuromuscular junction, Cell, 72/Neuron, 10(Suppl.), 99, 1993.
62. 3H] cytisine binding to human brain membrane preparations, Brain Res., 600, 127, 1993.
63. Halvorsen, S. W. and Berg, D. K., Subunit composition of nicotinic acetylcholine receptors from chick ciliary ganglia, J. Neurosci., 10, 1711, 1990.
64. Halvorsen, S. W., Schmid, H. A., McEachern, A. E. et al., Regulation of acetylcholine receptors on chick ciliary ganglion neurons by components from the synaptic target tissue, J. Neurosci., 11, 2177, 1991.
65. Henderson, L. P., Gdovin, M. J., Liu, C. L. et al., Nerve growth factor increases nicotinic ACh receptor gene expression and current density in wild-type and protein kinase A-deficient PC 12 cells, J. Neurosci., 14, 1153, 1994.
66. Hoover, F. and Goldman, D., Temporally correlated expression of nAChR genes during development of the mammalian retina, Exp. Eye Res., 54, 561, 1992.
67. 3H]-epibatidine binding to nicotinic cholinergic receptors in rat and human brain, Mol. Pharm., 48, 280, 1995.
68. Hu, M., Theobald, N. L. W., and Gardner, P. D., Nerve growth factor increases the transcriptional activity of the rat neuronal nicotinic acetylcholine receptor β4 subunit promoter in transfected PC12 cells, J. Neurochem., 62, 392, 1994.
69. Hulme, E. C., Birdsall, N. J. M., and Buckley, N. I., Muscarinic receptor subtypes, Ann. Rev. Pharmacol. Toxicol., 30, 633, 1991.
70. Ifune, C. K. and Steinbach, J. H., Regulation of sodium currents and acetylcholine responses in PC12 cells, Brain Res., 506, 243, 1990.
71. Jacob, M. H. and Berg, D. K., The ultrastructural localization of α-bungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons, J. Neurosci., 3, 260, 1983.
72. Jacob, M. H., Berg, D. K., and Lindstrom, J. M., Shared antigenic determinants between Electrophorus acetylcholine receptor and a synaptic component on chicken ciliary ganglion neurons, Proc. Natl. Acad. Sci. U.S.A., 81, 3223, 1984.
73. Jacob, M. H., Acetylcholine receptor expression in developing chick ciliary ganglion neurons, J. Neurosci., 11, 1701, 1991.
74. Karlin, A., Structure of nicotinic acetylcholine receptors, Curr. Opin. Neurobiol., 3, 299, 1993.
75. Kemp, G., Bentley, L., McNamee, M. G. et al., Purification and characterization of the α-bungarotoxin binding protein from rat brain, Brain Res., 347, 274, 1985.
76. Keyser, K. T., Britto, L. R. G., Schoepfer, R. et al., Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina, J. Neurosci., 13, 442, 1993.
77. Koyama, K., Sudo, K., and Nakamura, Y., Mapping of the human nicotinic acetylcholine receptor beta 3 gene (CHRNB3) within chromosome 8p11.2, Genomics, 21, 460, 1994.
78. Lamar, E., Miller, K., and Patrick, J., Amplification of genomic sequences identifies a new gene, alpha 6, in the nicotinic acetylcholine receptor gene family, Soc. Neuro. Abs., 16, 681, 1990.
79. Lena, C. and Changeux, J.-P., Allosteric modulations of the nicotinic acetylcholine receptor, TINS, 16, 181, 1993.
80. Le Novere, N. and Changeux, J.-P., Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells, J. Mol. Evolution, 40, 155, 1995.
81. Levey, M. S., Brumwell, C. L., Dryer, S. E. et al., Innervation and target tissue interactions differentially regulate acetylcholine receptor subunit mRNA levels in developing neurons in situ, Neuron, 14, 153, 1995.
82. Levin, E. D., Nicotinic systems and cognitive function, Psychopharmacology, 108, 417, 1992.
83. Lindstrom, J., Schoepfer, R., and Whiting, P., Molecular studies of the neuronal nicotinic acetylcholine receptor family, Mol. Neurobiol., 1, 281, 1987.
84. Listerud, M., Brussard, A. B., Devay, P. et al., Functional contribution of neuronal AChR subunits revealed by antisense nucleotides, Science, 254, 1518, 1991.
85. Liu, P.-S., Kao, L.-S., and Lin, M.-K., Organophosphates inhibit catecholamine secretion and calcium influx in bovine adrenal chromaffin cells. Toxicology, 90, 81, 1994.
86. Luetje, C. W., Wada, K., Rogers, S. et al., Neurotoxins distinguish between different neuronal acetylcholine receptor subunit combinalions. J. Neurochem., 55, 632, 1990.
87. Luetje, C. W. and Patrick, J., Both α- and β-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors, J. Neurosci., 11, 837, 1991.
88. Luetje, C. W., Piattoni, M., and Patrick, J., Mapping of ligand binding sites of neuronal nicotinic acetylcholine receptors using chimeric α subunits, Mol. Pharm., 44, 657, 1993.
89. Maconochie, D. J. and Knight, D. E., A study of the bovine adrenal chromaffin nicotinic receptor using patch clamp and concentration-jump techniques, J. Physiol. (Lond), 454, 129, 1992.
90. Madhok, T. C., Beyer, H. S., and Sharp, B. M., Protein kinase A regulates nicotinic cholinergic receptors and subunit messenger ribonucleic acids in PC12 cells, Endocrinology, 134, 91, 1994.
91. Mandelzys, A. and Cooper, E., Effects of ganglionic satellite cells and NGF on the expression of nicotinic acetylcholine currents by rat sensory neurons, J. Neurophysiol., 67, 1213, 1992.
92. Mandelzys, A., Pie, B., Deneris, E. S. et al., The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor α-subunit gene expression and occurs independent of innervation, J. Neurosci., 14, 2357, 1994.
93. Margiotta, J. F., Berg, D. K., and Dionne, V. E., The properties and regulation of functional acetylcholine receptors on chick ciliary ganglion neurons, J. Neurosci., 7, 3612, 1987a.
94. Margiotta, J. F., Berg, D. K., and Dionne, V. E., Cyclic AMP regulates the proportion of functional acetylcholine receptors on chicken ciliary ganglion neurons, Proc. Natl. Acad. Sci. U.S.A., 84, 8155, 1987b.
95. Marshall, L. M., Synaptic localization of α-bungarotoxin binding which blocks nicotinic transmission at frog sympathetic neurons, Proc. Natl. Acad. Sci. U.S.A., 78, 1948, 1981.
96. Matter, J.-M., Matter-Sadzinski, L., and Ballivet, M., Expression of neuronal nicotinic acetylcholine receptor genes in the developing chick visual system, EMBO J., 9, 1021, 1990.
97. Matter, J.-M., Matter-Sadzinski, L., and Ballivet, M., Activity of the β3 nicotinic receptor promoter is a marker of neuron fate determination during retina development, J. Neurosci., 15, 5919, 1995.
98. Matter-Sadzinski, L., Hernandez, M.-C., Roztocil, T. et al., Neuronal specificity of the α7 nicotinic acetylcholine receptor promoter develops during morphogenesis of the central nervous system, EMBO J., 11, 4529, 1992.
99. McEachern, A. E., Jacob, M. H., and Berg, D. K., Differential effects of nerve transections on the ACh and GABA receptors of chick ciliary ganglion neurons, J. Neurosci., 9, 3899, 1989.
100. McGehee, D. S. and Role, L. W., Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons, Ann. Rev. Physiol., 57, 521, 1995.
101. McGehee, D. S., Heath, M. J. S., Gelber, S. et al., Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science, 269, 1692, 1995.
102. Mihovilovic, M. and Roses, A. D., Expression of mRNAs in human thymus coding for the α3 subunit of a neuronal acetylcholine receptor, Exp. Neurol., 11, 175, 1991.
103. Mihovilovic, M., Hulette, C., Mittelstaedt, J. et al., Nicotinic neuronal acetylcholine receptor α3 subunit transcription in normal and myasthenic thymus, in Myasthenia Gravis and Related Disorders: Experimental and Clinical Aspects, Vol. 681 of the Annals of the New York Academy of Sciences, 1993, 83-96.
104. Mihovilovic, M., Mai, Y., Herbstreith, M. et al., Splicing of an anti-sense Alu sequence generates a coding sequence variant for the α-3 subunit of a neuronal acetylcholine receptor. Biochem. Biophys. Res. Comm., 197, 137, 1993.
105. Mihovilovic, M. and Roses, A. D., Expression of α-3, α-5, and β-4 neuronal acetylcholine receptor subunit transcripts in normal and myasthenia gravis thymus, J. Immunol. 151, 6517, 1993.
106. Miyai, I., Ueno, S., Yorifuji, S. et al., Alterations in neocortical expression of nicotinic acetylcholine receptor mRNAs following unilateral lesions of the rat nucleus basalis magnocellularis, J. Neurol. Trans., 82, 79, 1990.
107. Morley, B. J. and Happe, H. K., An in situ hybridization study of mRNA expression for α5 and α6, putative nicotinic acetylcholine receptor subunits, during postnatal development of the rat brain, Soc. Neurosci. Abs., 21, 1335, 1995.
108. Morris, B. J., Hicks, A. A., Wisden, W. et al., Distinct regional expression of nicotinic acetylcholine receptor genes in chick brain, Mol. Brain Res., 7, 305, 1990.
109. Moss, B. L., Schuetze, S. M., and Role, L. W., Functional properties and developmental regulation of nicotinic acetylcholine receptors on embryonic chicken sympathetic neurons. Neuron, 3, 597, 1989.
110. Mulle, C., Vidal, C., Benoit, P. et al., Existence of different subtypes of nicotinic acetylcholine receptors in the rat habenulo-interpeduncular system, J. Neurosci., 11, 2588, 1991.
111. Nakayama, H., Shirase, M., Nakashima, T. et al., Affinity purification of nicotinic acetylcholine receptor from rat brain, Mol. Brain Res., 7, 221, 1990.
112. Nakayama, H., Okuda, H., and Nakashima, T., Phosphorylation of rat brain nicotinic acetylcholine receptor by cAMP-dependent protein kinase in vitro. Mol. Brain. Res., 20, 171, 1993.
113. Nef, P., Oneyser, C., Alliod, C. et al., Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors, EMBO J., 7, 595, 1988.
114. Orr-Urtreger, A., Seidin, M. F., Baldini, A. et al., Cloning and mapping of the mouse alpha 7-neuronal nicotinic acetylcholine receptor, Genomics, 26, 399, 1995.
115. 3H] Cytisine binding to nicotinic cholinergic receptors in brain, Mol. Pharm., 39, 9, 1991.
116. Papke, R. L., Boulter, J., Patrick, J. et al., Single-channel currents of rat neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes, Neuron, 3, 589, 1989.
117. Papke, R. L. and Heinemann, S., The role of the β4-subunit in determining the kinetic properties of rat neuronal nicotinic acetylcholine α3-receptors, J. Physiol. (Lond), 440, 95, 1991.
118. Papke, R. L. The kinetic properties of neuronal nicotinic receptors: genetic basis of functional diversity, Prog. Neurobiol., 41, 509, 1993.
119. Papke, R. L. and Heinemann, S., Partial agonist properties of cytisine on neuronal nicotinic receptors containing the β2 subunit, Mol. Pharm., 45, 142, 1994.
120. Peng, X., Katz, M., Gerzanich, V. et. al., Human α7 acetylcholine receptor: cloning of the α7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional α7 homomers expressed in Xenopus oocytes, Mol. Pharm., 45, 546, 1994.
121. 3H]-epibatidine labels nicotinic receptors in rat brain: an autoradiographic study, JPET, 275, 1030, 1995.
122. Pugh, P. C. and Berg, D. K., Neuronal acetylcholine receptors that bind α-bungarotoxin mediate neunte retraction in a calcium-dependent manner, J. Neurosci., 14, 889, 1994.
123. Raimondi, E., Rubboli, F., Moralli, D. et al., Chromosomal localization and physical linkage of the genes encoding the human α3, α5, and β4 neuronal nicotinic receptor subunits, Genomics, 12, 849, 1992.
124. Revah, F., Bertrand, D., Galzi, J.-L. et al., Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor, Nature, 353, 846, 1991.
125. Rogers, S. W., Mandelzys, A., Deneris, E. S. et al., The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF, J. Neurosci., 12, 4611, 1992.
126. Role, L. W., Neural regulation of acetylcholine sensitivity in embryonic sympathetic neurons, Proc. Natl. Acad. Sci. U.S.A., 85, 2825, 1988.
127. Rothhut, B., Romano, S. J., Vijayaraghavan, S. et al., Posttranslational regulation of neuronal acetylcholine receptors stably expressed in a mouse fibroblast cell line, J. Neurobiol., 29, 115, 1996.
128. Rubboli, F., Court, J. A., Sala, C. et al., Distribution of neuronal nicotinic receptor subunits in human brain, Neurochem. Int., 25, 69, 1994.
129. Sands, S. B. and Barish, M. E., Calcium permeability of neuronal nicotinic acetylcholine receptor channels in PC12 cells, Brain Res., 560, 38, 1991.
130. Sargent, P. B. and Pang, D. Z., Acetylcholine receptor-like molecules are found in both synaptic and extrasynaptic clusters on the surface of neurons in the frog cardiac ganglion, J. Neurosci., 9, 1062, 1989.
131. Sargent, P. B., The diversity of neuronal nicotinic acetylcholine receptors, Ann. Rev. Neurosci., 16, 403, 1993.
132. Schoepfer, R., Whiting, P., Esch, F. et al., cDNA clones coding for the structural subunit of a chicken brain nicotinic acetylcholine receptor, Neuron, 1, 241, 1988.
133. Schoepfer, R., Halvorsen, S. W., Conroy, W. G. et al., Antisera against an acetylcholine receptor α3 fusion protein bind to ganglionic but not to brain acetylcholine receptors, FEBS Lett., 257, 393, 1989.
134. Schoepfer, R., Conroy, W. G., Whiting, P. et al., Brain α-bungarotoxin binding protein cDNAs and Mabs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily, Neuron, 5, 35, 1990.
135. Schuetze, S. M. and Role, L. W., Developmental regulation of nicotinic acetylcholine receptors, Ann. Rev. Neurosci., 10, 403, 1987.
136. Seguela, P., Wadiche, J., Dineley-Miller, K. et al., Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium, J. Neurosci., 13, 596, 1993.
137. Senba, E., Simmons, D. M., Wada, E. et al., RNA levels of neuronal nicotinic acetylcholine receptor subunits are differentially regulated in axotomized facial motoneurons: an in situ hybridization study, Mol. Brain Res., 8, 349, 1990.
138. Steinlein, O. K., Mulley, J. C., Propping, P. et al., A missense mutation in the neuronal nicotinic acetylcholine receptor α4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nature Genet., 11, 201, 1995.
139. Stollberg, J. and Berg, D. K., Neuronal acetylcholine receptors: fate of surface and internal pools in cell culture, J. Neurosci., 7, 1809, 1987.
140. Swanson, L. W., Simmons, D. M., Whiting, P. J. et al., Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system, J. Neurosci., 7, 3334, 1987.
141. Tzartos, S., Rand, D., Einarson, B. et al., Mapping of surface structure of Electrophorus acetylcholine receptor using monoclonal antibodies, J. Biol. Chem., 256, 8635, 1981.
142. Vernallis, A. B., Conroy, W. G., and Berg, D. K., Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes, Neuron, 10, 451, 1993.
143. Vernino, S., Amador, M., Luetje, C. W. et al., Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors, Neuron, 8, 127, 1992.
144. Vijayaraghavan S., Schmid, H. A., Halvorsen, S. W. et al., Cyclic AMP-dependent phosphorylation of a neuronal acetylcholine receptor α-type subunit, J. Neurosci., 10, 3255, 1990.
145. Wada, K., Ballivet, M., Boulter, J. et al., Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor, Science, 240, 330, 1988.
146. Wada, E., Wada, K., Boulter, J. et al., Distribution of alpha2, alpha3, alpha4, and beta2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat, J. Comp. Neural., 284, 314, 1989.
147. Wada, E., McKinnon, D., Heinemann, S. et al., The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (α5) in the rat central nervous system, Brain Res., 526, 45, 1990.
148. Wheeler, S. V., Chad, J. E., and Foreman, R., Residues 1 to 80 of the N-terminal domain of the β subunit confer neuronal bungarotoxin sensitivity and agonist selectivity on neuronal nicotinic receptors, FEBS Lett., 332, 139, 1993.
149. Whiting, P. J. and Lindstrom, J. M., Purification and characterization of a nicotinic acetylcholine receptor from chick brain, Biochemistry, 25, 2082, 1986a.
150. Whiting, P. J. and Lindstrom, J. M., Pharmacological properties of immuno-isolated neuronal nicotinic receptors, J. Neurosci., 6, 3061, 1986b.
151. Whiting, P. and Lindstrom, J. Affinity labeling of neuronal acetylcholine receptors localizes acetylcholine-binding sites to their β-subunits, FEBS Lett., 213, 55, 1987a.
152. Whiting, P. and Lindstrom, J., Purification and characterization of a nicotinic acetylcholine receptor from rat brain, Proc. Natl. Acad. Sci. U.S.A., 84, 595, 1987b.
153. Whiting, P. J., Liu, R., Morley, B. J. et al., Structurally different neuronal nicotinic acetylcholine receptor subtypes purified and characterized using monoclonal antibodies, J. Neurosci., 7, 4005, 1987a.
154. Whiting, P., Esch, F., Shimasaki, S. et al., Neuronal nicotinic acetylcholine receptor β subunit is coded for by the cDNA clone α4, FEBS Lett., 219, 459, 1987a.
155. Whiting, P. J., Schoepfer, R., Swanson, L. W. et al., Functional acetylcholine receptor in PC12 cells reacts with a monoclonal antibody to brain nicotinic receptors, Nature, 327, 515, 1987c.
156. Whiting, P. J. and Lindstrom, J., Characterization of bovine and human nicotinic acetylcholine receptors using monoclonal antibodies, J. Neurosci., 8, 3395, 1988.
157. Whiting, P. J., Schoepfer, R., Conroy, W. G. et al., Expression of nicotinic acetylcholine receptor subtypes in brain and retina, Mol. Brain Res., 10, 61, 1991.
158. Wonnacott, S., Drasdo, A., Sanderson, E. et al., Presynaptic nicotinic receptors and the modulation of transmitter release, Ciba Found. Symp., 152, 87, 1990.
159. Woolf, N. J., Cholinergic systems in mammalian brain and spinal cord. Progress in Neurobiol., 37, 475, 1991.
160. Yu, C. and Role, L. Antisense deletion reveals that α5 subunits participate in native chick neuronal nicotinic channels, Soc. Neurosci. Abs., 20, 1128 1994.
161. Zhang, Z-w., Vijayaraghavan, S., and Berg, D. K., Neuronal acetylcholine receptors that bind α-bungarotoxin with high affinity function as ligand-gated ion channels, Neuron, 12, 167, 1994.
162. Zheng, J. Q., Felder, M., Connor, J. A. et al., Turning of nerve growth cones induced by neurotransmitters, Nature, 368, 140, 1994.
163. Zoli, M., LeNovere, N., Hill, J. A., Jr. et al., Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems, J. Neurosci., 15, 1912, 1995.