Constructing inhibitory synapses

Nature Reviews Neuroscience

Volumn 2, Issue 4, 2001, Pages 240-250

  Moss, Stephen J ^a   Smart, Trevor G ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CARRIER PROTEIN; GEPHYRIN; GLYCINE RECEPTOR; MEMBRANE PROTEIN;

ANIMAL; CHANNEL GATING; CHEMISTRY; HUMAN; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT; REVIEW; SYNAPSE;

ANIMALS; CARRIER PROTEINS; HUMANS; ION CHANNEL GATING; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; SYNAPSES;

EID: 0035319805     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/35067500     Document Type: Article

References (143)

1. Schofield, P. R. et al. Sequence and functional expression of the GABAa receptor shows a ligand-gated receptor super- family. Nature 328, 221-227 (1987).
2. Grenningloh, G. et al. The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328, 215-220 (1987).
3. Maricq, A. V, Peterson, A. S., Brake, A. J., Myers, R. M. & Julius, D. Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science 254, 432-437 (1991).
4. Julius, D. Molecular biology of serotonin receptors. Annu. Rev. Neurosci. 14, 335-360 (1991).
5. Unwin, N. The nicotinic acetylcholine receptor of the Torpedo electric ray. J. Struct. Biol. 121, 181-190 (1998).
6. Grenningloh, G. et al. Alpha subunit variants of the human glycine receptor: primary structures, functional expression and chromosomal localization of the corresponding genes. EMBO J. 9, 771-776 (1990).
7. Betz, H. et al. Structure and functions of inhibitory and excitatory glycine receptors. Ann. NY Acad. Sci. 868, 667-676 (1999).
8. Harvey, R. J. & Betz, H. in Pharmacology of Ionic Channel Function: Activators and Inhibitors (eds Endo, M., Kurachi, Y. & Mishina, M.) 479-497 (Springer-Verlag, Berlin, 2000).
9. Kuhse, J. et al. Alternative splicing generates two isoforms of the a2 subunit of the inhibitory glycine receptor. FEBS Lett. 283, 73-77 (1991).
10. Langosch, D., Thomas, L. & Betz, H. Conserved quaternary structure of ligand-gated ion channels: the postsynaptic glycine receptor is a pentamer. Proc. Natl Acad. Sci. USA 85, 7394-7398 (1988).
11. Becker, C. M., Hoch, W. & Betz, H. Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J. 7, 3717-3726 (1988).
12. Bormann, J. & Feigenspan, A. GABAc receptors. Trends Neurosci. 18, 515-519 (1995).
13. Bormann, J. The 'ABC' of GABA receptors. Trends Pharmacol. Sci. 21, 16-19 (2000).
14. Sieghart, W. Unraveling the function of GABAa receptor subtypes. Trends Pharmacol. Sci. 21, 411-413 (2000).
15. Rabow, L. E., Russek, S. J. & Farb, D. H. From ion currents to genomic analysis: Recent advances in GABAa receptor research. Synapse 21, 189-274 (1996).
16. Davies, P A., Hanna, M. C., Hales, T. G. & Kirkness, E. F. lnsensitivity to anaesthetic agents conferred by a class of GABAa receptor subunit. Nature 385, 820-823 (1997).
17. Hedblom, E. & Kirkness, E. F. A novel class of GABAa receptor subunit in tissues of the reproductive system. J. Biol. Chem. 272, 15346-15350 (1997).
18. Bonnert, T. P et al. θ, a novel γ-aminobutyric acid type A receptor subunit. Proc. Natl Acad. Sci. USA 96, 9891-9896 (1999).
19. Laurie, D. J., Wisden, W. & Seeburg, P. H. The distribution of thirteen GABAa receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12, 4151-4172 (1992).
20. Fritschy, J.-M. & Mohler, H. GABAa receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol. 359, 154-194 (1995).
21. Connolly, C. N., Krishek, B. J., McDonald, B. J., Smart, T. G. & Moss, S. J. Assembly and cell surface expression of heteromeric and homomeric γ-aminobutyric acid type A receptors. J. Biol. Chem. 271, 89-96 (1996).
22. Gorrie, G. H. et al. Assembly of GABAAreceptors composed of α1 and β2 subunits in both cultured neurons and fibroblasts. J. Neurosci. 17, 6587-6596 (1997).
23. Taylor, P. M. et al. Identification of amino acid residues within GABAa receptor β subunits that mediate both homomeric and heteromeric receptor expression. J. Neurosci. 19, 6360-6371 (1999).
24. Taylor, P. M. et al. Identification of residues within GABA(A) receptor α subunits that mediate specific assembly with receptor β subunits. J. Neurosci. 20, 1297-1306 (2000).
25. 1subunit of the GABAa receptor forms a picrotoxin- sensitive anion channel open in the absence of GABA. FEBS Lett. 257, 377-379 (1989).
26. Krishek, B. J., Moss, S. J. & Smart, T. G. Homomeric β1 γ-aminobutyric acidA receptor-ion channels: evaluation of pharmacological and physiological properties. Mol. Pharmacol. 49, 494-504 (1996).
27. Wooltorton, J. R., Moss, S. J. & Smart, T. G. Pharmacological and physiological characterization of murine homomeric β3 GABAa receptors. Eur. J. Neurosci. 9, 2225-2235 (1997).
28. Connolly, C. N. et al. Subcellular localization and endocytosis of homomeric γ2 subunit splice variants of γ-aminobutyric acid type A receptors. Mol. Cell. Neurosci. 13, 259-271 (1999).
29. Sanna, E., Garau, F. & Harris, R. A. Novel properties of homomeric β1 γ-aminobutyric acid type A receptors: actions of the anesthetics propofol and pentobarbital. Mol. Pharmacol. 47, 213-217 (1995).
30. Pritchett, D. B. et al. Importance of a novel GABAa receptor subunit for benzodiazepine pharmacology. Nature 338, 582-585 (1989).
31. 2Ssubunits produce unique ion channels with dissimilar single- channel properties. J. Neurosci. 13, 1429-1440 (1993).
32. Chang, Y., Wang, R., Barot, S. & Weiss, D. S. Stoichiometry of a recombinant GABAa receptor. J. Neurosci. 16, 5415-5424 (1996).
33. Tretter, V, Ehya, N., Fuchs, K. & Sieghart, W. Stoichiometry and assembly of a recombinant GABAAreceptor subtype. J. Neurosci. 17, 2728-2737 (1997).
34. Farrar, S. J., Whiting, P J., Bonnert, T P & McKernan, R. M. Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J. Biol. Chem. 274, 10100-10104 (1999).
35. Shivers, B. D. et al. Two novel GABAa receptor subunits exist in distinct neuronal subpopulations. Neuron 3, 327-337 (1989).
36. Saxena, N. C. & MacDonald, R. L. Assembly of GABAa receptor subunits: role of the δ subunit. J. Neurosci. 14, 7077-7086 (1994).
37. Whiting, P J. et al. Neuronally restricted RNA splicing regulates the expression of a novel GABAa receptor subunit conferring atypical functional properties. J. Neurosci. 17, 5027-6037 (1997).
38. Rudolph, U. et al. Benzodiazepine actions mediated by specific γ-aminobutyric acidA receptor subtypes. Nature 401, 796-800 (1999).
39. Low, K. et al. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290, 131-134 (2000).
40. McKernan, R. M. et al. Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABAa receptor a1 subtype. Nature Neurosci. 3, 587-592 (2000).
41. Nusser, Z., Sieghart, W., Benke, D., Fritschy, J.-M. & Somogyi, P. Differential synaptic localization of two major γ-aminobutyric acid type A receptor a subunits on hippocampal pyramidal cells. Proc. Natl Acad. Sci. USA 93, 11939-11944 (1996).
42. Fritschy, J. M., Johnson, D. K., Mohler, H. & Rudolph, U. Independent assembly and subcellular targeting of GABAAreceptor subtypes demonstrated in mouse hippocampal and olfactory neurons in vivo. Neurosci. Lett. 249, 99-102 (1998).
43. 6 subunit gene inactivation inhibits 6 subunit expression. J. Neurosci. 17, 1350-1362 (1997).
44. Nusser, Z., Sieghart, W. & Somogyi, P. Segregation of different GABAa receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693-1703 (1998).
45. Sassoe-Pognetto, M., Panzanelli, P., Sieghart, W. & Fritschy, J. M. Co-localization of multiple GABAa receptor subtypes with gephyrin at postsynaptic sites. J. Comp Neurol. 420, 481-498 (2000).
46. Brickley, S. G., Cull-Candy, S. G. & Farrant, M. Single- channel properties of synaptic and extrasynaptic GABAa receptors suggest differential targeting of receptor subtypes. J. Neurosci. 19, 2960-2973 (1999).
47. Dotti, C. G., Parton, R. G. & Simons, K. Polarized sorting of glypiated proteins in hippocampal neurons. Nature 349, 158-161 (1991).
48. Jareb, M. & Banker, G. The polarized sorting of membrane proteins expressed in cultured hippocampal neurons using viral vectors. Neuron 20, 855-867 (1998).
49. Connolly, C. N., Wooltorton, J. R., Smart, T G. & Moss, S. J. Subcellular localization of γ-aminobutyric acid type A receptors is determined by receptor β-subunits. Proc. Natl Acad. Sci. USA 93, 9899-9904 (1996).
50. Cutting, G. R. et al. Cloning of the γ-aminobutyric acid (GABA) rho 1 cDNA: a GABA receptor subunit highly expressed in the retina. Proc. Natl Acad. Sci. USA 88, 2673-2677 (1991).
51. Lukasiewicz, P D. GABAc receptors in the vertebrate retina. Mol. Neurobiol. 12, 181-194 (1996).
52. Hackam, A. S., Wang, T.-L., Guggino, W. B. & Cutting, G. R. Sequences in the amino termini of GABA ρ and GABAa subunits specify their selective interaction in vitro. J. Neurochem. 70, 40-46 (1998).
53. Hackam, A. S., Guggino, W. B. & Cutting, G. R. The N-terminal domain of human GABA receptor p1 subunits contains signals for homooligomeric and heterooligomeric interaction. J. Biol. Chem. 272, 13750-13757 (1997).
54. Qian, H. & Ripps, H. Response kinetics and pharmacological properties of heteromeric receptors formed by coassembly of GABA ρ- and γ2-subunits. Proc. R. Soc. Lond. B 266, 2419-2425 (1999).
55. Pan, Z. H., Zhang, D., Zhang, X. & Lipton, S. A. Evidence for coassembly of mutant GABAc ρ1 with GABAa γ2S, glycine α1 and glycine α2 receptor subunits in vitro. Eur. J. Neurosci. 12, 3137-3145 (2000).
56. Koulen, P., Brandstatter, J. H., Enz, R., Bormann, J. & Wassle, H. Synaptic clustering of GABA(C) receptor rho- subunits in the rat retina. Eur. J. Neurosci. 10, 115-127 (1998).
57. Koulen, P. et al. Immunocytochemical localization of the GABAc receptor rho subunits in the cat, goldfish, and chicken retina. J. Comp. Neurol. 380, 520-532 (1997).
58. Schmitt, B., Knaus, P., Becker, C. M. & Betz, H. The Mr 93,000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 26, 805-811 (1987).
59. Johnson, J. L. & Wadman, S. K. in The Metabolic Basis of Inherited Diseases (eds Scrivner, C. R., Beaudef, A. L., Sly, W. S. & Valle, D.) 2271-2283 (McGraw-Hill, New York, 2001).
60. Prior, P et al. Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron 8, 1161-1170 (1992).
61. Ramming, M. et al. Diversity and phylogeny of gephyrin: tissue-specific splice variants, gene structure, and sequence similarities to molybdenum cofactor-synthesizing and cytoskeleton-associated proteins. Proc. Natl Acad. Sci. USA 97, 10266-10271 (2000).
62. Kirsch, J. & Betz, H. Widespread expression of gephyrin, a putative glycine receptor-tubulin linker protein, in rat brain. Brain Res. 621, 301-310 (1993).
63. Meyer, G., Kirsch, J., Betz, H. & Langosch, D. Identification of a gephyrin binding motif on the glycine receptor β subunit. Neuron 15, 563-572 (1995).
64. Kins, S., Kuhse, J., Laube, B., Betz, H. & Kirsch, J. Incorporation of a gephyrin-binding motif targets NMDA receptors to gephyrin-rich domains in HEK 293 cells. Eur. J. Neurosci. 11, 740-744 (1999).
65. Kneussel, M., Hermann, A., Kirsch, J. & Betz, H. Hydrophobic interactions mediate binding of the glycine receptor β-subunit to gephyrin. J. Neurochem. 72, 1323-1326 (1999).
66. Kirsch, J., Kuhse, J. & Betz, H. Targeting of glycine receptor subunits to gephryin-rich domains in transfected human embryonic kidney cells. Mol. Cell. Neurosci. 6, 450-461 (1995).
67. Kirsch, J. et al. The 93-kDa glycine receptor-associated protein binds to tubulin. J. Biol. Chem. 266, 22242-22245 (1991).
68. Kirsch, J., Wolters, I., Triller, A. & Betz, H. Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366, 745-748 (1993).
69. Feng, G. et al. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282, 1321-1324 (1998).
70. Sabatini, D. M. et al. Interaction of RAFT1 with gephyrin required for rapamycin-sensitive signaling. Science 284, 1161-1164 (1999).
71. Kins, S., Betz, H. & Kirsch, J. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nature Neurosci. 3, 22-29 (2000).
72. Reid, T., Bathoorn, A., Ahmadian, M. R. & Collard, J. G. Identification and characterization of hPEM-2, a guanine nucleotide exchange factor specific for Cdc42. J. Biol. Chem. 274, 33587-33593 (1999).
73. Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62 (1995).
74. Bishop, A. L. & Hall, A. Rho GTPases and their effector proteins. Biochem. J. 348, 241-255 (2000).
75. Van Aelst, L. & D'Souza-Schorey, C. Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322 (1997).
76. Mammoto, A. et al. Interactions of drebrin and gephyrin with profilin. Biochem. Biophys. Res. Commun. 243, 86-89 (1998).
77. Schluter, K., Jockusch, B. M. & Rothkegel, M. Profilins as regulators of actin dynamics. Biochim. Biophys. Acta 1359, 97-109 (1997).
78. Witke, W. et al. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17, 967-976 (1998).
79. Snyder, S. H. et al. Neural actions of immunophilin ligands. Trends Pharmacol. Sci. 19, 21-26 (1998).
80. Steward, O. mRNA localization in neurons: a multipurpose mechanism? Neuron 18, 9-12 (1997).
81. Racca, C., Gardiol, A. & Triller, A. Dendritic and postsynaptic localizations of glycine receptor a subunit mRNAs. J. Neurosci. 17, 1691-1700 (1997).
82. Kirsch, J. & Betz, H. Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature 392, 717-720 (1998).
83. Levi, S., Vannier, C. & Triller, A. Strychnine-sensitive stabilization of postsynaptic glycine receptor clusters. J. Cell Sci. 111, 335-345 (1998).
84. Areceptors and gephyrin expression in cultured motoneurons. J. Neurosci. 19, 7434-7449 (1999).
85. Taleb, O. & Betz, H. Expression of the human glycine receptor a1 subunit in Xenopus oocytes: apparent affinities of agonists increase at high receptor density. EMBO J. 13, 1318-1324 (1994).
86. Maammar, M., Rodeau, J. L. & Taleb, O. Permeation and gating of a1 glycine-gated channels expressed at low and high density in Xenopus oocyte. FEBS Lett. 414, 99-104 (1997).
87. Lim, R., Alvarez, F. J. & Walmsley, B. Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J. Physiol. 516, 505-512 (1999).
88. Item, C. & Sieghart, W. Binding of Y-aminobutyric acidA receptors to tubulin. J. Neurochem. 63, 1119-1125 (1994).
89. A receptors from bovine brain. J. Neurochem. 68, 1352-1360 (1997).
90. Triller, A., Cluzeaud, F. & Korn, H. Gamma-aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. J. Cell Biol. 104, 947-956 (1987).
91. Cabot, J. B., Bushnell, A., Alessi, V. & Mendell, N. R. Postsynaptic gephyrin immunoreactivity exhibits a nearly one-to-one correspondence with Y-aminobutyric acid-like immunogold-labeled synaptic inputs to sympathetic preganglionic neurons. J. Comp. Neurol. 356, 418-432 (1995).
92. Todd, A. J., Spike, R. C., Chong, D. & Neilson, M. The relationship between glycine and gephyrin in synapses of the rat spinal cord. Eur. J. Neurosci. 7, 1-11 (1995).
93. A-receptor subunits in the rat retina. J. Comp. Neurol. 357, 1-14 (1995).
94. Sassoe-Pognetto, M. & Fritschy, J. M. Mini-review: gephyrin, a major postsynaptic protein of GABAergic synapses. Eur. J. Neurosci. 12, 2205-2210 (2000).
95. Essrich, C., Lorez, M., Benson, J. A., Fritschy, J. M. & Luscher, B. Postsynaptic clustering of major GABAa receptor subtypes requires the γ2 subunit and gephyrin. Nature Neurosci. 1, 563-571 (1998).
96. Craig, A. M., Banker, G., Chang, W., McGrath, M. E. & Serpinskaya, A. S. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 16, 3166-3177 (1996).
97. Kneussel, M. et al. Loss of postsynaptic GABAa receptor clustering in gephyrin-deficient mice. J. Neurosci. 19, 9289-9297 (1999).
98. Baer, K. et al. Postsynaptic clustering of Y-aminobutyric acid type A receptors by the y3 subunit in vivo. Proc. Natl Acad. Sci. USA 96, 12860-12865 (1999).
99. Fischer, F. et al. Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J. Comp. Neurol. 427, 634-648 (2000).
100. Kirsch, J. & Betz, H. The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J. Neurosci. 15, 4148-4156 (1995).
101. Allison, D. W., Chervin, A. S., Gelfand, V. I. & Craig, A. M. Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J. Neurosci. 20, 4545-4554 (2000).
102. Meier, J., De Chaldee, M., Triller, A. & Vannier, C. Functional heterogeneity of gephyrins. Mol. Cell Neurosci. 16, 566-577 (2000).
103. Knuesel, I. et al. Short communication: altered synaptic clustering of GABAa receptors in mice lacking dystrophin (mdx mice). Eur. J. Neurosci. 11, 4457-4462 (1999).
104. A-receptor-associated protein links GABAa receptors and the cytoskeleton. Nature 397, 69-72 (1999).
105. A receptor interaction. J. Neurochem. 75, 644-655 (2000).
106. Mei, X., Sweatt, A. J. & Hammarback, J. A. Regulation of microtubule-associated protein 1B (MAP1B) subunit composition. J. Neurosci. Res. 62, 56-64 (2000).
107. Mann, S. S. & Hammarback, J. A. Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B. J. Biol. Chem. 269, 11492-11497 (1994).
108. Sagiv, Y, Legesse-Miller, A., Porat, A. & Elazar, Z. GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. EMBO J. 19, 1494-1504 (2000).
109. Legesse-Miller, A., Sagiv, Y., Glozman, R. & Elazar, Z. Aut7p, a soluble autophagic factor, participates in multiple membrane trafficking processes. J. Biol. Chem. 275, 32966-32973 (2000).
110. AR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc. Natl Acad. Sci. USA 97, 8594-8599 (2000).
111. A) receptor-associated protein (GABARAP) promotes GABA. receptor clustering and modulates the channel kinetics. Proc. Natl Acad. Sci. USA 97, 11557-11562 (2000).
112. Hanley, J. G., Koulen, P., Bedford, F., Gordon Weeks, P. R. & Moss, S. J. The protein MAP-1B links GABAc receptors to the cytoskeleton at retinal synapses. Nature 397, 66-69 (1999).
113. Hammarback, J. A. in Brain Microtubule Associated Proteins: Modifications in Disease (eds Avila, J., Kosik, K. & Brandt, R.) 1-17 (Harwood, Amsterdam, 2001).
114. Billups, D., Hanley, J. G., Orme, M., Attwell, D. & Moss, S. J. GABAc receptor sensitivity is modulated by interaction with MAP1B. J. Neurosci. 20, 8643-8650 (2000).
115. Hanley, J. G., Jones, E. M. & Moss, S. J. GABA receptor rho1 subunit interacts with a novel splice variant of the glycine transporter, GLYT-1. J. Biol. Chem. 275, 840-846 (2000).
116. Connolly, C. N. et al. Cell surface stability of Y-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J. Biol. Chem. 274, 36565-36572 (1999).
117. Chapell, R., Bueno, O. F., Alvarez-Hernandez, X., Robinson, L. C. & Leidenheimer, N. J. Activation of protein kinase C induces Y-aminobutyric acid type A receptor internalization in Xenopusoocytes. J. Biol. Chem. 273, 32595-32601 (1998).
118. Ghansah, E. & Weiss, D. S. Modulation of GABA. receptors by benzodiazepines and barbiturates is autonomous of PKC activation. Neuropharmacology 40, 327-333 (2001).
119. C) receptors by protein kinase C. Mol. Pharmacol. 57, 847-856 (2000).
120. Kittler, J. T. et al. Analysis of GABA. receptor assembly in mammalian cell lines and hippocampal neurons using y2 subunit green fluorescent protein chimeras. Mol. Cell. Neurosci. 16, 440-452 (2000).
121. Kittler, J. T. et al. Constitutive endocytosis of GABA. receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J. Neurosci. 20, 7972-7977 (2000).
122. Marsh, M. & McMahon, H. T The structural era of endocytosis. Science 285, 215-220 (1999).
123. Meyer, T. & Shen, K. In and out of the postsynaptic region: signalling proteins on the move. Trends Cell Biol. 10, 238-244 (2000).
124. Wan, Q. et al. Recruitment of functional GABA. receptors to postsynaptic domains by insulin. Nature 388, 686-690 (1997).
125. Moss, S. J. & Smart, T. G. Modulation of amino acid-gated ion channels by protein phosphorylation. Int. Rev. Neurobiol. 39, 1-52 (1996).
126. Smart, T. G. Regulation of excitatory and inhibitory neurotransmitter-gated ion channels by protein phosphorylation. Curr. Opin. Neurobiol. 7, 358-367 (1997).
127. McDonald, B. J. et al. Adjacent phosphorylation sites on GABA. receptor p subunits determine regulation by cAMP- dependent protein kinase. Nature Neurosci. 1, 23-28 (1998).
128. 2L subunits of the γ-aminobutyric acid type A receptor. J. Biol. Chem. 267, 14470-14476 (1992).
129. Moss, S. J., Smart, T. G., Blackstone, C. D. & Huganir, R. L. Functional modulation of GABA. receptors by cAMP- dependent protein phosphorylation. Science 257, 661-665 (1992).
130. McDonald, B. J. & Moss, S. J. Differential phosphorylation of intracellular domains of γ-aminobutyric acid type A receptor subunits by calcium/calmodulin type 2-dependent protein kinase and cGMP-dependent protein kinase. J. Biol. Chem. 269, 18111-18117 (1994).
131. 2+/calmodulin type II-dependent protein kinase. Neuropharmacology 36, 1377-1385 (1997).
132. Brandon, N. J. et al. Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J. Neurosci. 19, 9228-9234 (1999).
133. Mochly-Rosen, D. & Gordon, A. S. Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J. 12, 35-42 (1998).
134. Chang, B. Y, Conroy, K. B., Machleder, E. M. & Cartwright, C. A. RACK1, a receptor for activated C kinase and a homolog of the β subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18, 3245-3256 (1998).
135. Yarwood, S. J., Steele, M. R., Scotland, G., Houslay, M. D. & Bolger, G. B. The RACK1 signaling scaffold protein selectively interacts with the cAMP-specific phosphodiesterase PDE4D5 isoform. J. Biol. Chem. 274, 14909-14917 (1999).
136. Brandon, N. J. et al. GABA. receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J. Biol. Chem. 275, 38856-38862 (2000).
137. Smart, T. G., Thomas, P., Brandon, N. J. & Moss, S. J. in Pharmacology of GABA and Glycine Neurotransmission (ed. Mohler, H.) 195-225 (Springer-Verlag, Berlin, 2001).
138. Garner, C. C., Nash, J. & Huganir, R. L. PDZ domains in synapse assembly and signalling. Trends Cell Biol. 10, 274-280 (2000).
139. Ye, B. et al. GRASP-1: a neuronal RasGEF associated with the AMPA receptor/GRIP complex. Neuron 26, 603-617 (2000).
140. Kim, J. H., Liao, D., Lau, L. F. & Huganir, R. L. SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20, 683-691 (1998).
141. Noel, J. et al. Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23, 365-376 (1999).
142. Nishimune, A. et al. NSF binding to GluR2 regulates synaptic transmission. Neuron 21, 87-97 (1998).
143. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P. & Grant, S. G. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nature Neurosci. 3, 661–669 (2000).