Nicotinic α7 receptors: Synaptic options and downstream signaling in neurons

Journal of Neurobiology

Volumn 53, Issue 4, 2002, Pages 512-523

  Berg, Darwin K ^a   Conroy, William G ^a  

^a NEUROBIOLOGY SECTION   (United States)

Author keywords

7; Acetylcholine; Cholinergic; Ciliary; Hippocampus; Nicotinic; Receptor; Synaptic

Indexed keywords

ACETYLCHOLINE; CALCIUM; GENE PRODUCT; ION CHANNEL; LIGAND; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINIC RECEPTOR;

ARTICLE; CALCIUM MOBILIZATION; CHANNEL GATING; CHICKEN; CILIARY GANGLION; HIPPOCAMPUS; HUMAN; NERVOUS SYSTEM; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN; GANGLIA; NEURONS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 0036890808     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10116     Document Type: Article

References (130)

1. Alberini CM. 1999. Genes to remember. J Exp Biol 202:2887-2891.
2. Alkondon M, Albuquerque EX. 1993. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J Pharmacol Exp Ther 265:1455-1473.
3. Alkondon M, Pereira EFR, Albuquerque EX. 1998. α-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257-263.
4. Alkondon M, Pereira EFR, Barbosa CTF, Albuquerque EX. 1997a. Neuronal nicotinic acetylcholine receptor activation modulates γ-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 283:1396-1411.
5. Alkondon M, Pereira EFR, Cortes WS, Maelicke A, Albuquerque EX. 1997b. Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734-2742.
6. Arroyo-Jimenez MdM, Bourgeois J-P, Marubio LM, Le Sourd A-M, Ottersen OP, Rinvik E, Fairen A, Changeux J-P. 1999. Ultrastructural localization of the α4-subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra. J Neurosci 19:6475-6487.
7. Bertrand D, Galzi JL, Devillers-Thiéry A, Bertrand S, Changeux JP. 1993. Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc Natl Acad Sci USA 90:6971-6975.
8. 2+-dependent regulation in neuronal gene expression. Curr Opin Neurobiol 7:419-429.
9. Bruses JL, Chauvet N, Rutishauser U. 2001. Membrane lipid rafts are necessary for the maintenance of the α7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J Neurosci 21:504-512.
10. Buonanno A, Fields RD. 1999. Gene regulation by patterned electrical activity during neural and skeletal muscle development. Curr Opin Neurobiol 9:110-120.
11. Burns AL, Benson D, Howard MJ, Margiotta JF. 1997. Chick ciliary ganglion neurons contain transcripts coding for acetylcholine receptor-associated protein at synapses (rapsyn). J Neurosci 17:5016-5026.
12. Carroll RC, Lissin DV, von Zastrow M, Nicholl RA, Malenka RC. 1999. Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2:454-460.
13. Chalazonitis A, Zigmond RE. 1980. Effects of synaptic and antidromic stimulation of tyrosine hydroxylase activity in the rat superior cervical ganglion. J Physiol (Lond) 300: 525-538.
14. Chang K, Berg DK. 2001. Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons. Neuron 32:855-865.
15. Chen D, Patrick JW. 1997. The α-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the α7 subunit. J Biol Chem 272:24024-24029.
16. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA. 2001. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408:936-943.
17. Coggan JS, Paysan J, Conroy WG, Berg DK. 1997. Direct recording of nicotinic responses in presynaptic nerve terminals. J Neurosci 17:5798-5806.
18. Conroy WG, Berg DK. 1998. Nicotinic receptor subtypes in the developing chick brain: Appearance of a species containing the α4, β2, and α5 gene products. Mol Pharmacol 53:392-401.
19. Conroy WG, Berg DK. 1999. Rapsyn variants in ciliary ganglia and their possible effects on clustering of nicotinic receptors. J Neurochem 73:1399-1408.
20. 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 homooligomeric channel blocked by α-Btx. Neuron 5:847-856.
21. 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.
22. Cuevas J, Roth AL, Berg DK. 2000. Two distinct classes of functional α7-containing nicotinic receptors on rat superior cervical ganglion neurons. J Physiol (Lond) 525: 735-746.
23. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, Greenberg ME. 2000. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103:945-956.
24. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, Compton DK, Park JS, Smith C, DiStefano PS, Glass DJ, Burden SJ, Yancopoulos GD. 1996. The receptor tyrosine kinase, MuSK, is required for neuromuscular junction formation in vivo. Cell 85:501-512.
25. Deisseroth K, Bito H, Tsien RW. 1996. Signaling from synapse to nucleus: Postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16:89-101.
26. Descarries L. 1998. The hypothesis of an ambient level of acetylcholine in the central nervous system. J Physiol (Paris) 92:215-220.
27. Descarries L, Gisiger V, Steriade M. 1997. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53:603-625.
28. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME. 2001. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294:333-339.
29. Dourado M, Sargent PB. 2002. Properties of nicotinic receptors underlying Renshaw cell excitation by α-motor neurons in neonatal rat spinal cord. J Neurophysiol 87:3117-3125.
30. Drisdel RC, Green WN. 2000. Neuronal α-bungarotoxin receptors are α7 subunit homomers. J Neurosci 20:133-139.
31. Dryer S. 1994. Functional development of the parasympathetic neurons of the avian ciliary ganglion: A classic model system for the study of neuronal differentiation and development. Prog Neurobiol 43:281-322.
32. Eccles JC, Fatt P, Koketsu K. 1954. Cholinergic and inhibitory synapses in a pathway from motor axon collaterals to motoneurones. J Physiol (Lond) 126:524-562.
33. Fabian-Fine R, Skehel P, Errington 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.
34. Feng G, Steinbach JH, Sanes JR. 1998. Rapsyn clusters neuronal acetylcholine receptors but is inessential for formation of an interneuronal cholinergic synapse. J Neurosci 18:4166-4176.
35. 2+ channel-regulated neuronal gene expression. J Neurobiol 37:171-189.
36. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV. 1998. Synaptic potentials mediated via α-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18:8228-8235.
37. Frey U, Morris RG. 1997. Synaptic tagging and long-term potentiation. Nature 385:533-536.
38. Frotscher M, Leranth C. 1985. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study. J Comp Neurol 239:237-246.
39. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
40. Ghosh A, Ginty DD, Bading H, Greenberg ME. 1994. Calcium regulation of gene expression in neuronal cells. J Neurobiol 25:294-303.
41. Gingras J, Ferns M. 2001. Expression and localization of agrin during sympathetic synapse formation in vitro. J Neurobiol 48:228-242.
42. Goelet P, Castellucci VF, Schacher S, Kandel ER. 1986. The long and the short of long-term memory - A molecular framework. Nature 322:419-422.
43. Gotti C, Moretti M, Longhi R, Briscini L, Balestra B, Clementi F. 1994. Expression of α-bungarotoxin receptor subtypes in chick central nervous system during development. J Recept Res 14:335-346.
44. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
45. Greenberg ME, Ziff EB. 2001. Signal transduction in the postsynaptic neuron. Activity-dependent regulation of gene expression. In: Cowan WM, Sudhof TC, Stevens CF, editors. Synapses. Baltimore, MD: Johns Hopkins University Press, p 357-391.
46. Greenberg ME, Ziff EB, Greene LA. 1986. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234:80-83.
47. Gueorguiev VD, Zeman RJ, Meyer EM, Sabban EL. 2000. Involvement of α7 nicotinic acetylcholine receptors in activation of tyrosine hydroxylase and dopamine β-hydroxylase gene expression in PC12 cells. J Neurochem 75:1997-2005.
48. Halevi S, McKay J, Palfreyman M, Yassin L, Eshel M, Jorgensen E, Treinin M. 2002. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J 21:1012-1020.
49. Hanley JG, Khatri L, Hanson PI, Ziff EB. 2002. NSF ATPase and α-/β-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34:53-67.
50. Hardingham GE, Arnold FJL, Bading H. 2001. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4:261-267.
51. Hardingham GE, Fukunaga Y, Bading H. 2002. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414.
52. Hayashi Y, Shi SH, Esteban JA Piccini A, Poncer J-C, Malinow R. 2000. Driving AMPA receptors into synapses by LTP and CaMII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
53. Hefft S, Hulo S, Bertrand D, Muller D. 1999. Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol (Lond) 515:769-776.
54. Hu M, Liu Q-s, Chang KT, Berg DK. Nicotinic regulation of CREB activation in hippocampal neurons by glutamatergic and non-glutamatergic pathways. MCN, in press.
55. Huh K, Fuhrer C. 2001. Isolation of PICK1 as a binding substrate for α7 nicotinic receptors. Soc Neurosci Abstr 31:145.7.
56. Huh K-H, Fuhrer C. 2002. Clustering of nicotinic acetylcholine receptors: From the neuromuscular junction to interneuronal synapses. Mol Neurobiol 25:79-112.
57. Hung AY, Sheng M. 2002. PDZ domains: Structural modules for protein complex assembly. J Biol Chem 277:5699-5702.
58. Jacob MH, Berg DK. 1983. The ultrastructural localization of α-bungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons. J Neurosci 3:260-271.
59. Jacob MH, Berg DK, Lindstrom JM. 1984. A shared antigenic determinant between the Electrophorus acetylcholine receptor and a synaptic component on chick ciliary ganglion neurons. Proc Natl Acad Sci USA 81:3223-3227.
60. Jeanclos EM, Lin L, Treuil MW, Rao J, DeCoster MA, Anand R. 2001. The chaperone protein 14-3-3η interacts with the nicotinic acetylcholine receptor α4 subunit. J Biol Chem 276:28281-28290.
61. Jones S, Sudweeks S, Yakel JL. 1999. Nicotinic receptors in the brain: Correlating physiology with function. Trends Neurosci 22:555-561.
62. 3H]dopamine release in rat striatal slices via glutamate release. Mol Pharmacol 58:312-318.
63. A receptor responsiveness in cerebellar Purkinje neurons. J Neurosci 22:3969-3976.
64. Kawai H, Zago W, Berg DK. 2002. Nicotinic α7 receptor clusters on hippocampal GABAergic neurons: Regulation by synaptic activity and neurotrophins. J Neurosci 22:7903-7912.
65. Khiroug SS, Harkness PC, Lamb PW, Sudweeks SN, Khiroug L, Millar N, Yakel JL. 2002. Rat nicotinic ACh receptor α7 and β2 subunits co-assemble to form functional heteromeric nicotinic receptor channels. J Physiol (Lond) 540:425-434.
66. Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Shibasaki H, Kume T, Akaike A. 2001. α7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block a β-amyloid-induced neurotoxicity. J Biol Chem 276:13541-13546.
67. Kornau H-C, Schenker LT, Kennedy MB, Seeburg PH. 1995. Domain interaction between NMDA receptor sub-units and the postsynaptic density protein PSD-95. Science 269:1737-1740.
68. 2+-dependent inactivation of NMDA receptors. J Neurosci 19:1165-1178.
69. Legendre P, Rosenmund C, Westbrook GL. 1993. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13:674-684.
70. Lein ES, Schatz CJ. 2000. Rapid regulation of brain-derived neurotrophic factor mRNA within eye-specific circuits during ocular dominance column formation. J Neurosci 20:1470-1483.
71. Lena C, Changeux J-P, Mulle C. 1993. Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J Neurosci 13:2680-2688.
72. Levy RB, Aoki C. 2002. α7 nicotinic acetylcholine receptors occur at postsynaptic densities of AMPA receptor-positive and -negative excitatory synapses in rat sensory cortex. J Neurosci 22:5001-5015.
73. Lindstrom J. 1996. Neuronal nicotinic acetylcholine receptors. In: Narahashi T, editor. Ion channels, vol 4. New York: Plenum Press, p 377-450.
74. Liu Q-s, Berg DK. 1999. Actin filaments and the opposing actions of CaM kinase II and calcineurin in regulating α7-containing nicotinic receptors on chick ciliary ganglion neurons. J Neurosci 19:10280-10288.
75. 125I-toxin F binding sites on chick ciliary neurons: Synaptic localization of a toxin that blocks ganglionic nicotinic receptors. J Neurosci 7:2153-2162.
76. Loring RH, Dahm RH, Zigmond RE. 1985. Localization of α-bungarotoxin binding sites in the ciliary ganglion of the embryonic chick: An autoradiographic study at the light and electron microscopic level. Neurosci 14:645-660.
77. Luscher C, Xia H, Beattie EC, Carroll RC, von Sastrow M, Malenka RC, Nicoll RA. 1999. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649-658.
78. Maggi L, Sher E, Cherubini E. 2001. Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J Physiol (Lond) 536:89-100.
79. McGehee D, Heath M, Gelber S, Role LW. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1697.
80. McKinney M, Coyle JT, Hedreen JC. 1983. Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217:103-121.
81. McMahon LL, Yoon K-W, Chiappinelli VA. 1994. Nicotinic receptor activation facilitates GABAergic neurotransmission in the avian lateral spiriform nucleus. Neuroscience 59:689-698.
82. Mermelstein PG, Bito H, Deisseroth K, Tsien RW. 2000. Critical dependence of cAMP response element-binding protein phosphorylation of L-type calcium channels supports a selective response to EPSPs in preference to action potentials. J Neurosci 20:266-273.
83. Mittaud P, Marangi PA, Erb-Vogtli S, Fuhrer C. 2001. Agrin-induced activation of acetylcholine receptor-bound Src family kinases requires rapsyn and correlates with acetylcholine receptor clustering. J Biol Chem 276:14505-14513.
84. Mohamed AS, Swope SL. 1999. Phosphorylation and cytoskeletal anchoring of the acetylcholine receptor Src class protein-tyrosine kinases. J Biol Chem 274:20529-20539.
85. Mohamed AS, Rivas-Plata KA, Draas JR, Saleh SM, Swope SL. 2001. Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J Neurosci 21:3806-3818.
86. 2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20:389-399.
87. Nguyen PV, Abel T, Kandel ER. 1994. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
88. Niethammer M, Kim E, Sheng M. 1996. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 16:2157-2163.
89. Nishimune A, Isaac JTR, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM. 1998. NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
90. O'Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, Worley P. 1999. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23:309-323.
91. O'Brien R, Xu D, Mi R, Tang X, Hopf C, Worley P. 2002. Synaptically targeted Narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons. J Neurosci 22:4487-4498.
92. Osten P, Srivastava S, Inman GJ, Vilim FS, Khatri L, Lee LM, States BA, Einheber S, Milner TA, Hanson PI, Ziff EB. 1998. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and α- and β-SNAPs. Neuron 21:99-110.
93. Papke RL, Bencherif M, Lippiello R. 1996. An evaluation of neuronal nicotinic acetylcholine receptor activation by quaternary nitrogen compounds indicates that choline is selective for the α7 subtype. Neurosci Lett 213:201-204.
94. Pelto-Huikko M, Dagerlind A, Kononen J, Lundberg JM, Villar M, Koistinaho J, Bravo R, Hokfelt T. 1995. Neuronal regulation of c-Fos, c-jun, and junB immediate-early genes in rat adrenal medulla. J Neurosci 15:1854-1868.
95. 2+ channels are essential for glutamate-mediated CREB phosphorylation and c-fos gene expression in striatal neurons. J Neurosci 19:6348-6359.
96. 3 receptors in developing visual cortex. J Neurosci 17:8353-8362.
97. Role LW, Berg DK. 1996. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077-1085.
98. Rosenmund R, Westbrook GL. 1993a. Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10:805-814.
99. 2+ and ATP. J Physiol (Lond) 470:705-729.
100. Salminen O, Seppa T, Gaddnas H, Ahtee L. 1999. The effects of acute nicotine on the metabolism of dopamine and the expression of Fos protein in striatal and limbic brain areas of rats during chronic nicotine infusion and its withdrawal. J Neurosci 19:8145-8151.
101. Sargent PB. 1993. The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403-443.
102. 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.
103. 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.
104. Sheng M, Sala C. 2001. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1-29.
105. Shoop RD, Martone ME, Yamada N, Ellisman MH, Berg DK. 1999. Neuronal acetylcholine receptors with α7 sub-units are concentrated on somatic spines for synaptic signaling in embryonic chick ciliary ganglia. J Neurosci 19:692-704.
106. Shoop RD, Chang KT, Ellisman MH, Berg DK. 2001. Synaptically-driven calcium transients via nicotinic receptors on somatic spines. J Neurosci 21:771-781.
107. Shoop RD, Esquenazi E, Yamada N, Ellisman MH, Berg DK. 2002. Ultrastructure of a somatic spine mat for nicotinic signaling in neurons. J Neurosci 22:748-756.
108. Shoop RD, Yamada N, Berg DK. 2000. Cytoskeletal links of neuronal acetylcholine receptors containing α7 subunits. J Neurosci 20:4021-4029.
109. Stanley EF. 1993. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11:1007-1011.
110. Tomita S, Nicoll RA, Bredt DS. 2001. PDZ protein interactions regulating glutamate receptor function and plasticity. J Cell Biol 153:F19-F23.
111. Tsen G, Williams B, Allaire P, Zhou Y-D, Ikonomov O, Kondova I, Jacob MH. 2000. Receptors with opposing functions are in postsynaptic microdomains under one presynaptic terminal. Nat Neurosci 3:126-132.
112. Turrini P, Casu MA, Wong TP, De Koninck Y, Ribeiro-Da-Silva A, Cuello AC. 2001. Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: Synaptic pattern and age-related atrophy. Neuroscience 105:277-285.
113. Ullian EM, McIntosh JM, Sargent PB. 1997. Rapid synaptic transmission in the avian CG is mediated by two distinct classes of nicotinic receptors. J Neurosci 17:7210-7219.
114. van Hoek ML, Allen CS, Parsons SJ. 1997. Phosphotyrosine phosphatase activity associated with c-Src in large multimeric complexes isolated from adrenal medullary chromaffin cells. Biochem J 326:271-277.
115. Vernallis AB, Conroy WG, Berg DK. 1993. Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451-464.
116. Vogt KE, Regehr WG. 2001. Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21:75-83.
117. Westbrook GL, Krupp JL, Vissel B. 1997. Cytoskeletal interactions with glutamate receptors at central synapses. In: Froehner SH, Bennett GV, editors. Cytoskeletal Regulation of Membrane Function. New York: Rockefeller University Press, p 163-175.
118. Williams BM, Tamburni MK, Schwartz Levey M, Bertrand S, Bertrand D, Jacob MH. 1998. The long internal loop of the α3 subunit targets nAChRs to subdomains within individual synapses on neurons in vivo. Nat Neurosci 1:557-562.
119. Wilson Horch HL, Sargent PB. 1995. Perisynaptic surface distribution of multiple classes of nicotinic acetylcholine receptors on neurons in the chicken ciliary ganglion. J Neurosci 15:7778-7795.
120. Wonnacott S. 1997. Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92-98.
121. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M. 1997. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385:439-442.
122. Yoshikami D, Bagabaldo Z, Olivera BM. 1989. The inhibitory effects of omega-conotoxins on Ca channels and synapses. Ann NY Acad Sci 560:230-248.
123. Yu CR, Role LW. 1998. Functional contribution of the α7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones. J Physiol (Lond) 509:651-665.
124. Zarei MM, Radcliffe KA, Chen D, Patrick JW, Dani JA. 1999. Distributions of nicotinic acetylcholine receptor α7 and 2 subunits on cultured hippocampal neurons. Neuroscience 88:755-764.
125. Zhang M, Wang YT, Vyas DM, Neuman RS, Bieger D. 1993. Nicotinic cholinoceptor-mediated excitatory postsynaptic potentials in rat nucleus ambiguus. Exp Brain Res 96:83-88.
126. Zhang S, Ehlers MD, Bernhardt JP, Su C-T, Huganir RL. 1998. Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21:443-453.
127. Zhang Z-w, Coggan JS, Berg DK. 1996. Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17:1231-1240.
128. Zhang Z-w, Vijayaraghavan S, Berg DK. 1994. Neuronal acetylcholine receptors that bind α-bungarotoxin with high affinity function as ligand-gated ion channels. Neuron 12:167-177.
129. Zoli M, Jansson A, Sykova E, Agnati LF, Fuxe K. 1999. Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol Sci 20: 142-150.
130. Zorumski CF, Thio LL, Isenberg KE, Clifford DB. 1992. Nicotinic acetylcholine currents in cultured postnatal rat hippocampal neurons. Mol Pharmacol 41:931-936.