GABAA receptors: Properties and trafficking

Critical Reviews in Biochemistry and Molecular Biology

Volumn 42, Issue 1, 2007, Pages 3-14

  Michels, Guido ^a,b,c   Moss, Stephen J ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Benzodiazepines; Clathrin; Endocytosis; GABARAP; Gamma aminobutyric acid; Gephyrin; Ligand gated ion channels; Plic 1

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 7 CHLORO 5 (2 FLUOROPHENYL) 1,3 DIHYDRO 1 (2,2,2 TRIFLUOROETHYL) 2H 1,4 BENZODIAZEPIN 2 ONE; ANESTHETIC AGENT; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE; BETA CARBOLINE DERIVATIVE; CHLORIDE CHANNEL; DIAZEPAM; ENZYME; GABA A RECEPTOR ASSOCIATED PROTEIN; GEPHYRIN; GLUTAMATE RECEPTOR INTERACTING PROTEIN 1; HUNTINGTIN ASSOCIATED PROTEIN 1; IMIDAZOPYRIDINE DERIVATIVE; N ETHYLMALEIMIDE SENSITIVE FACTOR; PHOSPHOLIPASE C RELATED CATALYTICALLY INACTIVE PROTEIN 1; PLIC 1 PROTEIN; PROTEIN; QUAZEPAM; TRIAZOLOPYRIDAZINE DERIVATIVE; UNC 51 LIKE KINASE; UNCLASSIFIED DRUG; ZALEPLON; ZOLPIDEM;

AMINO TERMINAL SEQUENCE; ANTIBODY LABELING; AUTORADIOGRAPHY; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL TYPE; CLUSTER ANALYSIS; DRUG BINDING; ENDOCYTOSIS; EXOCYTOSIS; NONHUMAN; PALMITOYLATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; ENDOCYTOSIS; HUMANS; PROTEIN TRANSPORT; RECEPTORS, GABA-A;

EID: 33847790372     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.1080/10409230601146219     Document Type: Review

References (93)

1. Beck, M., Brickley, K., Wilkinson, H.L., Sharma, S., Smith, M., Chazot, P.L., Pollard, S., and Stephenson, F.A. 2002. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem 277:30079-30090.
2. Bedford, F.K., Kittler, J.T., Muller, E., Thomas, P., Uren, J.M., Merlo, D., Wisden, W., Triller, A., Smart, T.G., and Moss, S.J. 2001. GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci 4:908-916.
3. Belelli, D. and Lambert, J.J. 2005. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6:565-575.
4. Benson, J.A., Low, K., Keist, R., Mohler, H., and Rudolph, U. 1998. Pharmacology of recombinant gamma-aminobutyric acidA receptors rendered diazepam-insensitive by point-mutated alpha-subunits. FEBS Lett 431:400-404.
5. Bogdanov, Y., Michels, G., Armstrong-Gold, C., Haydon, P.G., Lindstrom, J., Pangalos, M., and Moss, S.J. 2006. Synaptic GABA(A) receptors are directly recruited from their extrasynaptic counterparts. Embo J
6. Bonnert, T.P., McKernan, R.M., Farrar, S., le Bourdelles, B., Heavens, R.P., Smith, D.W., Hewson, L., Rigby, M.R., Sirinathsinghji, D.J., Brown, N., et al. 1999. theta, a novel gamma-aminobutyric acid type A receptor subunit. Proc Natl Acad Sci USA 96:9891-9896.
7. Brandon, N.J. and Moss, S.J. 2000. Receptor cross talk: ligand-gated ion channels start to communicate. Sci STKE 2000: PE1
8. Brickley, K., Smith, M.J., Beck, M., and Stephenson, F.A. 2005. GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem 280:14723-14732.
9. Brickley, S.G., Cull-Candy, S.G., and Farrant, M. 1999. Single-channel properties of synaptic and extrasynaptic GABAA receptors suggest differential targeting of receptor subtypes. J Neurosci 19:2960-2973.
10. Caraiscos, V.B., Elliott, E.M., You-Ten, K.E., Cheng, V.Y., Belelli, D., Newell, J.G., Jackson, M.F., Lambert, J.J., Rosahl, T.W., Wafford, K.A., et al. 2004. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 101:3662-3667.
11. Chang, Y., Wang, R., Barot, S., and Weiss, D.S. 1996. Stoichiometry of a recombinant GABAA receptor. J Neurosci 16:5415-5424.
12. Charych, E.I., Yu, W., Miralles, C.P., Serwanski, D.R., Li, X., Rubio, M., and De Blas, A.L. 2004. The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J Neurochem 90173-189.
13. Chavas, J., Forero, M.E., Collin, T., Llano, I., and Marty, A. 2004. Osmotic tension as a possible link between GABA(A) receptor activation and intracellular calcium elevation. Neuron 44:701-713.
14. Cinar, H. and Barnes, E.M., Jr. 2001. Clathrin-independent endocytosis of GABA(A) receptors in HEK 293 cells. Biochemistry 40:14030-14036.
15. Connolly, C.N., Krishek, B.J., McDonald, B.J., Smart, T.G., and Moss, S.J. 1996. Assembly and cell surface expression of heteromeric and homomeric gamma-aminobutyric acid type A receptors. J Biol Chem 271:89-96.
16. Connolly, C.N., Uren, J.M., Thomas, P., Gorrie, G.H., Gibson, A., Smart, T.G., and Moss, S.J. 1999. Subcellular localization and endocytosis of homomeric gamma2 subunit splice variants of gamma-aminobutyric acid type A receptors. Mol Cell Neurosci 13:259-271.
17. Connolly, C.N., Wooltorton, J.R., Smart, T.G., and Moss, S.J. 1996. Subcellular localization of gamma-aminobutyric acid type A receptors is determined by receptor beta subunits. Proc Natl Acad Sci USA 93:9899-9904.
18. Crestani, F., Low, K., Keist, R., Mandelli, M., Mohler, H., and Rudolph, U. 2001. Molecular targets for the myorelaxant action of diazepam. Mol Pharmacol 59:442-445.
19. Davies, P.A., Hanna, M.C., Hales, T.G., and Kirkness, E.F. 1997. Insensitivity to anaesthetic agents conferred by a class of GABA(A) receptor subunit. Nature 385:820-823.
20. DiAntonio, A. and Hicke, L. 2004. Ubiquitin-dependent regulation of the synapse. Annu Rev Neurosci 27:223-246.
21. Dong, H., O'Brien, R.J., Fung, E.T., Lanahan, A.A., Worley, P.F., and Huganir, R.L. 1997. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386:279-284.
22. Duncalfe, L.L., Carpenter, M.R., Smillie, L.B., Martin, I.L., and Dunn, S.M. 1996. The major site of photoaffinity labeling of the gamma-aminobutyric acid type A receptor by [3 H]flunitrazepam is histidine 102 of the alpha subunit. J Biol Chem 271:9209-9214.
23. Engelender, S., Sharp, A.H., Colomer, V., Tokito, M.K., Lanahan, A., Worley, P., Holzbaur, E.L., and Ross, C.A. 1997. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum Mol Genet 6:2205-2212.
24. Essrich, C., Lorez, M., Benson, J.A., Fritschy, J.M., and Luscher, B. 1998. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1:563-571.
25. Farrant,M. and Nusser, Z. 2005. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
26. Fisher, J.L. and Macdonald, R.L. 1997. Single channel properties of recombinant GABAA receptors containing gamma 2 or delta subtypes expressed with alpha 1 and beta 3 subtypes in mouse L929 cells. J Physiol. 505 (Pt 2): 283-297.
27. Fritschy, J.M., Johnson, D.K., Mohler, H., and Rudolph, U. 1998. Independent assembly and subcellular targeting of GABA(A)-receptor subtypes demonstrated in mouse hippocampal and olfactory neurons in vivo. Neurosci Lett 249:99-102.
28. Fritschy, J.M. and Mohler, H. 1995. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154-194.
29. Gauthier, L.R., Charrin, B.C., Borrell-Pages, M., Dompierre, J.P., Rangone, H., Cordelieres, F.P., De Mey, J., MacDonald, M.E., Lessmann, V., Humbert, S., et al. 2004. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118:127-138.
30. Gilbert, S.L., Zhang, L., Forster, M.L., Anderson, J.R., Iwase, T., Soliven, B., Donahue, L.R., Sweet, H.O., Bronson, R.T., Davisson, M.T., et al. 2006. Trak1 mutation disrupts GABA(A) receptor homeostasis in hypertonic mice. Nat Genet 38:245-250.
31. Goto, H., Terunuma, M., Kanematsu, T., Misumi, Y., Moss, S.J., and Hirata, M. 2005. Direct interaction of N-ethylmaleimide-sensitive factor with GABA(A) receptor beta subunits. Mol Cell Neurosci 30:197-206.
32. Herring, D., Huang, R., Singh, M., Robinson, L.C., Dillon, G.H., and Leidenheimer, N.J. 2003. Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor. J Biol Chem 278:24046-24052.
33. Jacob, T.C., Bogdanov, Y.D., Magnus, C., Saliba, R.S., Kittler, J.T., Haydon, P.G., and Moss, S.J. 2005. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci 25:10469-10478.
34. Jarolimek, W., Lewen, A., and Misgeld, U. 1999. A furosemide-sensitive K+-Cl- cotransporter counteracts intracellular Cl- accumulation and depletion in cultured rat midbrain neurons. J Neurosci 19:4695-4704.
35. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J 19:5720-5728.
36. Kaila, K. 1994. Ionic basis of GABAA receptor channel function in the nervous system. Prog Neurobiol 42:489-537.
37. Kanematsu, T., Jang, I.S., Yamaguchi, T., Nagahama, H., Yoshimura, K., Hidaka, K., Matsuda, M., Takeuchi, H., Misumi, Y., Nakayama, K., et al. 2002. Role of the PLC-related, catalytically inactive protein p130 in GABA(A) receptor function. Embo J 21:1004-1011.
38. Kanematsu, T., Takeuchi, H., Terunuma, M., and Hirata, M. 2005. PRIP, a novel Ins(1,4,5)P3 binding protein, functional significance in Ca2+ signaling and extension to neuroscience and beyond. Mol Cells 20:305-314.
39. Keller, C.A., Yuan, X., Panzanelli, P., Martin, M.L., Alldred, M., Sassoe-Pognetto, M., and Luscher, B. 2004. The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J Neurosci 24:5881-5891.
40. Kittler, J.T., Arancibia-Carcamo, I.L., and Moss, S.J. 2004. Association of GRIP1 with a GABA(A) receptor associated protein suggests a role for GRIP1 at inhibitory synapses. Biochem Pharmacol 68:1649-1654.
41. Kittler, J.T., Chen, G., Honing, S., Bogdanov, Y., McAinsh, K., Arancibia-Carcamo, I.L., Jovanovic, J.N., Pangalos, M.N., Haucke, V., Yan, Z., et al. 2005. Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci USA 102:14871-14876.
42. Kittler, J.T., Delmas, P., Jovanovic, J.N., Brown, D.A., Smart, T.G., and Moss, S.J. 2000. Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20:7972-7977.
43. Kittler, J.T., Rostaing, P., Schiavo, G., Fritschy, J.M., Olsen, R., Triller, A., and Moss, S.J. 2001. The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABA(A) receptors. Mol Cell Neurosci 18:13-25.
44. Kittler, J.T., Thomas, P., Tretter, V., Bogdanov, Y.D., Haucke, V., Smart, T.G., and Moss, S.J. 2004. Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci USA 101:12736-12741.
45. Kneussel, M., Brandstatter, J.H., Laube, B., Stahl, S., Muller, U., and Betz, H. 1999. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19:9289-9297.
46. Korpi, E.R. and Sinkkonen, S.T. 2006. GABA(A) receptor subtypes as targets for neuropsychiatric drug development. Pharmacol Ther 109:12-32.
47. Krishek, B.J., Moss, S.J., and Smart, T.G. 1996. Homomeric beta 1 gamma-aminobutyric acid A receptor-ion channels: evaluation of pharmacological and physiological properties. Mol Pharmacol 49:494-504.
48. Laurie, D.J., Wisden, W., and Seeburg, P.H. 1992. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
49. Le Roy, C. and Wrana, J.L. 2005. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112-126.
50. Li, R.W., Serwanski, D.R., Miralles, C.P., Li, X., Charych, E., Riquelme, R., Huganir, R.L., and de Blas, A.L. 2005. GRIP1 in GABAergic synapses. J Comp Neurol 488:11-27.
51. Li, S.H., Gutekunst, C.A., Hersch, S.M., and Li, X.J. 1998. Interaction of huntingtin-associated protein with dynactin P150Glued. J Neurosci 18:1261-1269.
52. Lorez, M., Benke, D., Luscher, B., Mohler, H., and Benson, J.A. 2000. Single-channel properties of neuronal GABAA receptors from mice lacking the 2 subunit. J Physiol. 527(Pt 1):11-31.
53. Low, K., Crestani, F., Keist, R., Benke, D., Brunig, I., Benson, J.A., Fritschy, J.M., Rulicke, T., Bluethmann, H.,Mohler, H., et al. 2000. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290:131-134.
54. Lu, J., Karadsheh, M., and Delpire, E. 1999. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39:558-568.
55. Luddens, H., Pritchett, D.B., Kohler, M., Killisch, I., Keinanen, K., Monyer, H., Sprengel, R., and Seeburg, P.H. 1990. Cerebellar GABAA receptor selective for a behavioural alcohol antagonist. Nature 346:648-651.
56. Luscher, B. and Keller, C.A. 2004. Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 102:195-221.
57. Malminiemi, O. and Korpi, E.R. 1989. Diazepam-insensitive [3H]Ro 15-4513 binding in intact cultured cerebellar granule cells. Eur J Pharmacol 169:53-60.
58. Marsh, M. and McMahon, H.T. 1999. The structural era of endocytosis. Science 285:215-220.
59. McKernan, R.M. and Whiting, P.J. 1996. Which GABAA-receptor subtypes really occur in the brain?. Trends Neurosci 19:139-143.
60. Mohammadi, B., Krampfl, K., Petri, S., Bogdanova, D., Kossev, A., Bufler, J., and Dengler, R. 2006. Selective and nonselective benzodiazepine agonists have different effects on motor cortex excitability. Muscle Nerve 33:778-784.
61. Moss, S.J. and Smart, T.G. 2001. Constructing inhibitory synapses. Nat Rev Neurosci 2:240-250.
62. Nichols, B.J. 2002. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat Cell Biol 4:374-378.
63. Nusser, Z., Sieghart, W., Benke, D., Fritschy, J.M., and Somogyi, P. 1996. Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93:11939-11944.
64. Okazaki, N., Yan, J., Yuasa, S., Ueno, T., Kominami, E., Masuho, Y., Koga, H., and Muramatsu, M. 2000. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res 85:1-12.
65. Pirker, S., Schwarzer, C., Wieselthaler, A., Sieghart, W., and Sperk, G. 2000. GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
66. Prior, P., Schmitt, B., Grenningloh, G., Pribilla, I., Multhaup, G., Beyreuther, K., Maulet, Y., Werner, P., Langosch, D., Kirsch, J., et al. 1992. Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron 8:1161-1170.
67. Pritchett, D.B., Sontheimer, H., Shivers, B.D., Ymer, S., Kettenmann, H., Schofield, P.R., and Seeburg, P.H. 1989. Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338:582-585.
68. Quinlan, J.J., Homanics, G.E., and Firestone, L.L. 1998. Anesthesia sensitivity in mice that lack the beta3 subunit of the gamma-aminobutyric acid type A receptor. Anesthesiology 88:775-780.
69. Rathenberg, J., Kittler, J.T., and Moss, S.J. 2004. Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol Cell Neurosci 26:251-257.
70. Rudolph, U. and Antkowiak, B. 2004. Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5:709-720.
71. Rudolph, U., Crestani, F., Benke, D., Brunig, I., Benson, J.A., Fritschy, J.M., Martin, J.R., Bluethmann, H., and Mohler, H. 1999. Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401:796-800.
72. Rudolph, U. and Mohler, H. 2006. GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol 6:18-23.
73. Sagiv, Y., Legesse-Miller, A., Porat, A., and Elazar, Z. 2000. GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. Embo J 19:1494-1504.
74. Schmid, S.L. 1997. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem 66:511-548.
75. Schofield, P.R., Darlison, M.G., Fujita, N., Burt, D.R., Stephenson, F.A., Rodriguez, H., Rhee, L.M., Ramachandran, J., Reale, V., Glencorse, T.A., et al. 1987. Sequence and functional expression of the GABA A receptor shows a ligand-gated receptor super-family. Nature 328:221-227.
76. Shivers, B.D., Killisch, I., Sprengel, R., Sontheimer, H., Kohler, M., Schofield, P.R., and Seeburg, P.H. 1989. Two novel GABAA receptor subunits exist in distinct neuronal subpopulations. Neuron 3:327-337.
77. Sieghart, W. 1989. Multiplicity of GABAA-benzodiazepine receptors. Trends Pharmacol Sci 10:407-411.
78. Sieghart, W. 1995. Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes. Pharmacol Rev 47:181-234.
79. Sieghart, W. and Sperk, G. 2002. Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem 2:795-816.
80. Sigel, E., Baur, R., Trube, G., Mohler, H., andMalherbe, P. 1990. The effect of subunit composition of rat brain GABAA receptors on channel function. Neuron 5:703-711.
81. Takei, K., Slepnev, V.I., Haucke, V., and De Camilli, P. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33-39.
82. Tanida, I., Komatsu, M., Ueno, T., and Kominami, E. 2003. GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3. Biochem Biophys Res Commun 300:637-644.
83. Terunuma, M., Jang, I.S., Ha, S.H., Kittler, J.T., Kanematsu, T., Jovanovic, J.N., Nakayama, K.I., Akaike, N., Ryu, S.H., Moss, S.J., et al. 2004. GABAA receptor phospho-dependent modulation is regulated by phospholipase C-related inactive protein type 1, a novel protein phosphatase 1 anchoring protein. J Neurosci 24:7074-7084.
84. Thomas, P., Mortensen, M., Hosie, A.M., and Smart, T.G. 2005. Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neurosci 8:889-897.
85. Thompson, S.A., Wheat, L., Brown, N.A., Wingrove, P.B., Pillai, G.V., Whiting, P.J., Adkins, C., Woodward, C.H., Smith, A.J., Simpson, P.B., et al. 2004. Salicylidene salicylhydrazide, a selective inhibitor of beta 1-containing GABAA receptors. Br J Pharmacol 142:97-106.
86. Tretter, V., Ehya, N., Fuchs, K., and Sieghart, W. 1997. Stoichiometry and assembly of a recombinant GABAA receptor subtype. J Neurosci 17:2728-2737.
87. Vardi, N., Zhang, L.L., Payne, J.A., and Sterling, P. 2000. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J Neurosci 20:7657-7663.
88. Wallner,M., Hanchar, H.J., and Olsen, R.W. 2003. Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci USA 100:15218-15223.
89. Wang, H., Bedford, F.K., Brandon, N.J., Moss, S.J., and Olsen, R.W. 1999. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397:69-72.
90. Wei, W., Faria, L.C., and Mody, I. 2004. Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABAA receptors in hippocampal neurons. J Neurosci 24:8379-8382.
91. Weimer, R.M., Richmond, J.E., Davis, W.S., Hadwiger, G., Nonet, M.L., and Jorgensen, E.M. 2003. Defects in synaptic vesicle docking in unc-18 mutants. Nat Neurosci 6:1023-1030.
92. Wisden, W., Laurie, D.J., Monyer, H., and Seeburg, P.H. 1992. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
93. Wisden, W. and Moss, S.J. 1997. gamma-Aminobutyric acid type A receptor subunit assembly and sorting: gene targeting and cell biology approaches. Biochem Soc Trans 25:820-824.