Mechanisms of GABAA receptor assembly and trafficking: Implications for the modulation of inhibitory neurotransmission

Molecular Neurobiology

Volumn 26, Issue 2-3, 2002, Pages 251-268

  Kittler, Josef T ^a   McAinsh, Kristina ^a   Moss, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

AP2; Assembly; Clathrin; Dynamin; Endocytosis; Endoplasmic reticulum; ER; GABA; GABARAP; Gephyrin; Inhibitory; Ion channel; NSF; PLIC; Receptor; Synapse; Targeting

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID C RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ANXIOLYTIC AGENT; CELL PROTEIN; HYPNOTIC AGENT; RECEPTOR PROTEIN; SEDATIVE AGENT;

ANXIETY DISORDER; ARTICLE; CELL SURFACE; CENTRAL NERVOUS SYSTEM; DEPRESSION; DYNAMICS; EPILEPSY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; INOTROPISM; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUBSTANCE ABUSE; SYNAPSE; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; NERVE CELL INHIBITION; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW;

ANIMALS; HUMANS; NEURAL INHIBITION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION;

EID: 0036771570     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1385/MN:26:2-3:251     Document Type: Article

References (132)

1. Couve, A., Moss, S. J., and Pangalos, M. N. (2000) GABAB receptors: A new paradigm in G protein signaling. Mol. Cell Neurosci. 16(4),. 296-312.
2. Moss, S. J. and Smart, T. G. (2001) Constructing inhibitory synapses. Nat. Rev. Neurosci. 2(4), 240-250.
3. Macdonald, R. L. and Olsen, R. W. (1994) GABAA receptor channels. Annu. Rev. Neurosci. 17, 569-602.
4. Rabow, L. E., Russek, S. J., and Farb, D. H. (1995) From ion currents to genomic analysis: Recent advances in GABAA receptor research. Synapse 21(3), 189-274.
5. Chandler, L. J., Harris, R. A., and Crews, F. T. (1998) Ethanol tolerance and synaptic plasticity. Trends Pharmacol. Sci. 19(12), 491-495.
6. Wallace, R. H., Marini, C., Petrou, S., et al. (2001) Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat. Genet. 28(1), 49-52.
7. Baulac, S., Huberfeld, G., Gourfinkel-An, I., et al. (2001) First genetic evidence of GABA(A) receptor dysfunction in epilepsy: A mutation in the gamma2-subunit gene. Nat. Genet. 28(1), 46-48.
8. Bateson, A. N. (2002) Basic pharmacologic mechanisms involved in benzodiazepine tolerance and withdrawal. Curr. Pharm. Des. 8(1), 5-21.
9. Ortells, M. O. and Lunt, G. G. (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci. 18(3), 121-127.
10. 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(6619), 820-823.
11. Hedblom, E. and Kirkness, E. F. (1997) A novel class of GABAA receptor subunit in tissues of the reproductive system. J. Biol. Chem. 272(24), 15,346-15,350.
12. Bormann, J. (2000) The 'ABC' of GABA receptors. Trends Pharmacol. Sci. 21(1), 16-19.
13. 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(3), 1040-1062.
14. 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(11), 4151-4172
15. 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(1), 154-194.
16. 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. Neuro-science 101(4), 815-850.
17. 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(3), 494-504.
18. Davies, P. A., Kirkness, E. F., and Hales, T. G. (1997) Modulation by general anaesthetics of rat GABAA receptors comprised of alpha 1 beta 3 and beta 3 subunits expressed in human embryonic kidney 293 cells. Br. J. Pharmacol. 120(5), 899-909.
19. 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(18), 9899-9904.
20. Wooltorton, J. R., Moss, S. J., and Smart, T. G. (1997) Pharmacological and physiological characterization of murine homomeric beta3 GABA(A) receptors. Eur. J. Neurosci. 9(11), 2225-2235.
21. Pritchett, D. B., Sontheimer, H., Shivers, B. D., et al. (1989) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338(6216), 582-585.
22. Shivers, B. D., Killisch, I., Sprengel, R., et al. (1989) Two novel GABAA receptor subunits exist in distinct neuronal subpopulations. Neuron 3(3), 327-337.
23. 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(1), 89-96.
24. Levitan, E. S., Schofield, P. R., Burt, D. R., et al. (1988) Structural and functional basis for GABAA receptor heterogeneity. Nature 335(6185), 76-79.
25. Levitan, E. S., Blair, L. A., Dionne, V. E., and Barnard, E. A. (1988) Biophysical and pharmacological properties of cloned GABAA receptor subunits expressed in Xenopus oocytes. Neuron 1(9), 773-781.
26. Schofield, P. R., Darlison, M. G., Fujita, N., et al. (1987) Sequence and functional expression of the GABA A receptor shows a ligandgated receptor super-family. Nature 328(6127), 221-227.
27. +. Neuron 5(6), 781-788.
28. a. Pritchett, D. B., Luddens, H., and Seeburg, P. H. (1989) Type I and type II GABAA-benzodia-zepine receptors produced in transfected cells. Science 245(4924), 1389-1392.
29. Tretter, V., Ehya, N., Fuchs, K., and Sieghart, W. (1997) Stoichiometry and assembly of a recombinant GABAA receptor subtype. J. Neurosci. 17(8), 2728-2737.
30. Vicini, S., Ferguson, C., Prybylowski, K., Kralic, J., Morrow, A. L., and Homanics, G. E. (2001) GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J. Neurosci. 21(9), 3009-3016.
31. Sur, C., Wafford, K. A., Reynolds, D. S., et al. (2000) Loss of the major GABA(A) receptor subtype in the brain is not lethal in mice. J. Neurosci. 21(10), 3409-3418.
32. Brickley, S. G., Revilla, V., Cull-Candy, S. G., Wisden, W., and Farrant, M. (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409(6816), 88-92.
33. Tretter, V., Hauer, B., Nusser, Z., et al. (2001) Targeted disruption of the GABA(A) receptor delta subunit gene leads to an up-regulation of gamma 2 subunit-containing receptors in cerebellar granule cells. J. Biol. Chem. 276(13), 10,532-10,538.
34. a. Homanics, G. E., DeLorey, T. M., Firestone, L. L., et al. (1997) Mice devoid of gamma-aminobu-tyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc. Natl. Acad. Sci. USA 94(8), 4143-4148.
35. b. DeLorey, T. M., Handforth, A., Anagnostaras, S. G., et al. (1998) Mice lacking the beta3 subunit of the GABAA receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J. Neurosci. 18(20), 8505-8514.
36. c. Gunther, U., Benson, J., Benke, D., et al. (1995) Benzodiazepine-insensitive mice generated by targeted disruption of the gamma 2 subunit gene of gamma-aminobutyric acid type A receptors. Synaptic control of glycine and GABA(A) receptors and gephyrin expression in cultured motoneurons. Proc. Natl. Acad. Sci. USA 92(17), 7749-7753.
37. Saxena, N. C. and Macdonald, R. L. (1996) Properties of putative cerebellar gamma-aminobutyric acid A receptor isoforms. Mol. Pharmacol. 49(3), 567-579.
38. Saxena, N. C. and Macdonald, R. L. (1994) Assembly of GABAA receptor subunits: Role of the delta subunit. J. Neurosci. 14(11 Pt 2), 7077-7086.
39. Margeta-Mitrovic, M., Jan, Y. N., and Jan, L. Y. (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27(1), 97-106.
40. Green, W. N. and Millar, N. S. (1995) Ion-channel assembly. Trends Neurosci. 18(6), 280-287.
41. Couve, A., Filippov, A. K., Connolly, C. N., Bettler, B., Brown, D. A., and Moss, S. J. (1998) Intracellular retention of recombinant GABAB receptors. J. Biol. Chem. 273(41), 26,361-26,367.
42. Standley, S., Roche, K. W., McCallum, J., Sans, N., and Wenthold, R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28(3), 887-898.
43. Angelotti, T. P. and Macdonald, R. L. (1993) Assembly of GABAA receptor subunits: Alpha 1 beta 1 and alpha 1 beta 1 gamma 25 subunits produce unique ion channels with dissimilar single-channel properties. J. Neurosci. 13(4), 1429-1440.
44. Taylor, P. M., Connolly, C. N., Kittler, J. T., et al. (2000) Identification of residues within GABA(A) receptor alpha subunits that mediate specific assembly with receptor beta sub-units. J. Neurosci. 20(4), 1297-1306.
45. Connolly, C. N., Uren, J. M., Thomas, P., et al. (1999) Subcellular localization and endocytosis of homomeric gamma2 subunit splice variants of gamma-aminobutyric acid type A receptors. Mol. Cell Neurosci. 13(4), 259-271.
46. Gorrie, G. H., Vallis, Y., Stephenson, A., et al. (1997) Assembly of GABAA receptors composed of alpha1 and beta2 subunits in both cultured neurons and fibroblasts. J. Neurosci. 17(17), 6587-6596.
47. Hammond, C. and Helenius, A. (1994) Folding of VSV G protein: Sequential interaction with BiP and calnexin. Science 266(5184), 456-458.
48. Whiting, P., McKernan, R. M., and Iversen, L. L. (1990) Another mechanism for creating diversity in gamma-aminobutyrate type A receptors: RNA splicing directs expression of two forms of gamma 2 phosphorylation site. Proc. Natl. Acad. Sci. USA 87(24), 9966-9970.
49. Kofuji, P., Wang, J. B., Moss, S. J., Huganir, R. L., and Burt, D. R. (1991) Generation of two forms of the gamma-aminobutyric acidA receptor gamma 2-subunit in mice by alternative splic ing. J. Neurochem. 56(2), 713-715.
50. Connolly, C. N., Kittler, J. T., Thomas, P., et al. (1999) Cell surface stability of gamma-aminobu-tyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J. Biol. Chem. 274(51), 36,565-13,572.
51. Kittler, J. T., Wang, J., Connolly, C. N., Vicini, S., Smart, T. G., and Moss, S. J. (2000) Analysis of GABAA receptor assembly in mammalian cell lines and hippocampal neurons using gamma 2 subunit green fluorescent protein chimeras. Mol. Cell Neurosci. 16(4), 440-452.
52. Taylor, P. M., Thomas, P., Gorrie, G. H., et al. (1999) Identification of amino acid residues within GABA(A) receptor beta subunits that mediate both homomeric and heteromeric receptor expression. J. Neurosci. 19(15), 6360-6371.
53. Gardiol, A., Racca, C., and Triller, A. (1999) Dendritic and postsynaptic protein synthetic machinery. J. Neurosci. 19(1), 168-179.
54. Racca, C., Gardiol, A., and Triller, A. (1997) Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs. J. Neurosci. 17(5), 1691-1700.
55. Klausberger, T., Fuchs, K., Mayer, B., Ehya, N., and Sieghart, W. (2000) GABA(A) receptor assembly. Identification and structure of gamma(2) sequences forming the intersubunit contacts with alpha(1) and beta(3) subunits. J. Biol. Chem. 275(12), 8921-8928.
56. Klausberger, T., Ehya, N., Fuchs, K., Fuchs, T., Ebert, V., Sarto, I., and Sieghart, W. (2001) Detection and binding properties of GABA(A) receptor assembly intermediates. J. Biol. Chem. 276(19), 16,024-16,032.
57. Klausberger, T., Sarto, I., Ehya, N., et al. (2001) Alternate use of distinct intersubunit contacts controls GABAA receptor assembly and stoichiometry. J. Neurosci. 21(23), 9124-9133.
58. Srinivasan, S., Nichols, C. J., Lawless, G. M., Olsen, R. W., and Tobin, A. J. (1999) Two invariant tryptophans on the alpha1 subunit define domains necessary for GABA(A) receptor assembly. J. Biol. Chem. 274(38), 26,633-26,638.
59. Smith, G. B. and Olsen, R. W. (1994) Identification of a [3H]muscimol photoaffinity substrate in the bovine gamma-aminobutyric acidA receptor alpha subunit. J. Biol. Chem. 269(32), 20,380-20,387.
60. Rudolph, U., Crestani, F., Benke, D., et al. (1999) Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401(6755), 796-800.
61. Rudolph, U., Crestani, F., and Mohler, H. (2001) GABA(A) receptor subtypes: Dissecting their pharmacological functions. Trends Pharmacol. Sci. 22(4), 188-194.
62. Nusser, Z., Sieghart, W., Benke, D., Fritschy, J. M., and Somogyi, P. (1996) Differential synaptic localization of two major gamma-aminobu-tyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 93(21), 11,939-11,944.
63. 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(2-3), 99-102.
64. Koulen, P., Sassoe-Pognetto, M., Grunert, U., and Wassle, H. (1996) Selective clustering of GABA(A) and glycine receptors in the mammalian retina. J. Neurosci. 16(6), 2127-2140.
65. Nusser, Z., Sieghart, W., Stephenson, F. A., and Somogyi, P. (1996) The alpha 6 subunit of the GABAA receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J. Neurosci. 16(1), 103-114.
66. Nusser, Z., Sieghart, W., and Somogyi, P. (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18(5), 1693-1703.
67. 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(8), 2960-2973.
68. Banks, M. I. and Pearce, R. A. (2000) Kinetic differences between synaptic and extrasynaptic GABA(A) receptors in CA1 pyramidal cells. J. Neurosci. 20(3), 937-948.
69. Brickley, S. G., Cull-Candy, S. G., and Farrant, M. (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J. Physiol. (Lond.) 497(Pt 3), 753-759.
70. Wall, M. J. and Usowicz, M. M. (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur. J. Neurosci. 9(3), 533-548.
71. Rossi, D. J. and Hamann, M. (1998) Spillover-mediated Transmission at Inhibitory Synapses Promoted by High Affinity Alpha6 Subunit GABA(A) Receptors and Glomerular Geometry [published erratum appears in Neuron 1998 July, 21(1), 527].
72. Jones, A., Korpi, E. R., McKernan, R. M., et al. (1997) Ligand-gated ion channel subunit partnerships: GABAA receptor alpha6 subunit gene inactivation inhibits delta subunit expression. J. Neurosci. 17(4), 1350-1362.
73. Hamann, M., Rossi, D. J., and Attwell, D. (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33(4), 625-633.
74. Jessell, T. M. and Kandel, E. R. (1993) Synaptic transmission: A bidirectional and self-modifiable form of cell-cell communication. Cell 72(Suppl), 1-30.
75. Bliss, T. V. and Collingridge, G. L. (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361(6407), 31-39.
76. Busch, C. and Sakmann, B. (1990) Synaptic transmission in hippocampal neurons: Numerical reconstruction of quantal IPSCs. Cold Spring Harb. Symp. Quant. Biol. 55, 69-80.
77. Redman, S. (1990) Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70(1), 165-198.
78. Tong, G. and Jahr, C. E. (1994) Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12(1), 51-59.
79. Edwards, F. A. (1995) Anatomy and electro-physiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 75(4), 759-787.
80. Mody, I., De Koninck, Y., Otis, T. S., and Soltesz, I. (1994) Bridging the cleft at GABA synapses in the brain. Trends Neurosci. 17(12), 517-525.
81. Nusser, Z., Cull-Candy, S., and Farrant, M. (1997) Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19(3), 697-709.
82. Nusser, Z., Hajos, N., Somogyi, P., and Mody, I. (1998) Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395(6698), 172-177.
83. Otis, T. S., De Koninck, Y., and Mody, I. (1994) Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Natl. Acad. Sci. USA 91(16), 7698-7702.
84. Wan, Q., Xiong, Z. G., Man, H. Y., et al. (1997) Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388(6643), 686-690.
85. Brunig, I., Penschuck, S., Berninger, B., Benson, J., and Fritschy, J. M. (2001) BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABA(A) recep tor surface expression. Eur. J. Neurosci. 13(7), 1320-1328.
86. 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(21), 7972-7977.
87. Chu, P., Murray, S., Lissin, D., and von Zastrow, M. (1997) Delta and kappa opioid receptors are differentially regulated by dynamin-dependent endocytosis when activated by the same alkaloid agonist. J. Biol. Chem. 272(43), 27,124-27,130.
88. Pitcher, J. A., Freedman, N. J., and Lefkowitz, R. J. (1998) G protein-coupled receptor kinases. Annu. Rev. Biochem. 67, 653-692.
89. Carroll, R. C., Beattie, E. C., Xia, H., et al. (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc. Natl. Acad. Sci. USA 96(24), 14,112-14,117.
90. Carroll, R. C., Beattie, E. C., von Zastrow, M., and Malenka, R. C. (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev. Neurosci. 2(5), 315-324.
91. Luscher, C., Xia, H., Beattie, E. C., et al. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24(3), 649-658.
92. Man, H. Y., Lin, J. W., Ju, W. H., et al. (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25(3), 649-662.
93. Marsh, M. and McMahon, H. T. (1999) The structural era of endocytosis. Science 285(5425), 215-220.
94. Tehrani, M. H. and Barnes, E. M., Jr. (1993) Identification of GABAA/enzodiazepine receptors on clathrin-coated vesicles from rat brain. J. Neurochem. 60(5), 1755-1761.
95. Tehrani, M. H., Baumgartner, B. J., and Barnes, E. M., Jr. (1997) Clathrin-coated vesicles from bovine brain contain uncoupled GABAA receptors. Brain Res. 776(1-2), 195-203.
96. Tehrani, M. H. and Barnes, E. M., Jr. (1997) Sequestration of gamma-aminobutyric acidA receptors on clathrin-coated vesicles during chronic benzodiazepine administration in vivo. J. Pharmacol. Exp. Ther. 283(1), 384-390.
97. Tehrani, M. H. and Barnes, E. M., Jr. (1991) Agonist-dependent internalization of gamma-aminobutyric acidA/enzodiazepine receptors in chick cortical neurons. J. Neurochem. 57(4), 1307-1312.
98. 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(7), 563-571.
99. Crestani, F., Lorez, M., Baer, K., et al. (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat. Neurosci. 2(9), 833-839.
100. Kneussel, M. and Betz, H. (2000) Clustering of inhibitory neurotransmitter receptors at developing postsynaptic sites: The membrane activation model. Trends Neurosci. 23(9), 429-435.
101. Kittler, J. T. and Moss, S. J. (2001) Neurotransmitter receptor trafficking and the regulation of synaptic strength. Traffic 2(7), 437-448.
102. 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(21), 9289-9297.
103. a. Levi, S., Chesnoy-Marchais, D., Sieghart, W., and Triller, A. (1999) Synaptic control of glycine and GABA(A) receptors and gephyrin expression in cultured motoneurons. J. Neurosci. 19(17), 7434-7449.
104. b. Campos, M. L., de Cabo, C., Wisden, W., Juiz, J. M., and Merlo, D. (2001) Expression of GABA(A) receptor subunits in rat brainstem auditory pathways: Cochlear nuclei, superior olivary complex and nucleus of the lateral lemniscus. Neuroscience 102(3), 625-638.
105. 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(6714), 69-72.
106. Hanley, J. G., Koulen, P., Bedford, F., Gordon-Weeks, P. R., and Moss, S. J. (1999) The protein MAP-1B links GABA(C) receptors to the cytoskeleton at retinal synapses. Nature 397(6714), 66-69.
107. Bedford, F. K., Kittler, J. T., Muller, E., et al. (2001) GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat. Neurosci. 4(9), 908-916.
108. a. Kins, S., Betz, H., and Kirsch, J. (2000) Colly-bistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat. Neurosci. 3(1), 22-29.
109. b. Mammoto, A., Sasaki, T., Asakura, T., et al. (1998) Interactions of drebrin and gephyrin with profilin. Biochem. Biophys. Res. Commun. 243(1), 86-89.
110. Nymann-Andersen, J., Wang, H., Chen, L., Kittler, J. T., Moss, S. J., and Olsen, R. W. (2002) Subunit specificity and interaction domain between GABA(A) receptor-associated protein (GABARAP) and GABA(A) receptors. J. Neurochem. 80(5), 815-823.
111. Ohsumi, Y. (2001) Molecular dissection of autophagy: Two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2(3), 211-216.
112. 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(7), 1494-1504.
113. 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(1), 13-25.
114. Kabeya, Y., Mizushima, N., Ueno, T., et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19(21), 5720-5728.
115. Wang, H. and Olsen, R. W. (2000) Binding of the GABA(A) receptor-associated protein (GABARAP) to microtubules and micro- filaments suggests involvement of the cytoskeleton in GABARAPGABA(A) receptor interaction. J. Neurochem. 75(2), 644-655.
116. Coyle, J. E., Qamar, S., Rajashankar, K. R., and Nikolov, D. B. (2002) Structure of GABARAP in two conformations: Implications for GABA(A) receptor localization and tubulin binding. Neuron 33(1), 63-74.
117. Chen, L., Wang, H., Vicini, S., and Olsen, R. W. (2000) The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc. Natl. Acad. Sci. USA 97(21), 11,557-11,562.
118. Kneussel, M., Haverkamp, S., Fuhrmann, J. C., Wang, H., Wassle, H., Olsen, R. W., and Betz, H. (2000) The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc. Natl. Acad. Sci. USA 97(15), 8594-8599.
119. Passafaro, M. and Sheng, M. (1999) Synapto-genesis: The MAP location of GABA receptors Curr. Biol. 9(7), R261-R263.
120. Knight, D., Harris, R., McAlister, M. S., et al. (2002) The X-ray crystal structure and putative ligand-derived peptide binding properties of gamma-aminobutyric acid receptor type A receptor-associated protein. J. Biol. Chem. 277(7), 5556-5561.
121. Phillips, W. D. and Froehner, S. C. (2002) GABARAP and GABA(A) receptor clustering. Neuron 33(1), 4-6.
122. Kanematsu, T., Jang, I. S., Yamaguchi, T., et al. (2002) Role of the PLC-related, catalytically inactive protein p130 in GABA(A) receptor function. EMBO J. 21(5), 1004-1011.
123. Wu, A. L., Wang, J., Zheleznyak, A., and Brown, E. J. (1999) Ubiquitin-related proteins regulate interaction of vimentin intermediate filaments with the plasma membrane. Mol. Cell 4(4), 619-625.
124. Luscher, B. and Keller, C. A. (2001) Ubiquitination, proteasomes and GABA(A) receptors. Nat. Cell. Biol. 3(10), E232-E233.
125. Mah, A. L., Perry, G., Smith, M. A., and Monteiro, M. J. (2000) Identification of ubiquilin, a novel presenilin interactor that increases presenilin protein accumulation. J. Cell. Biol. 151(4), 847-862.
126. Kleijnen, M. F., Shih, A. H., Zhou, P., Kumar, S., Soccio, R. E., Kedersha, N. L., Gill, G., and Howley, P. M. (2000) The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome. Mol. Cell 6(2), 409-419.
127. Caillard, O., Ben-Ari, Y., and Gaiarsa, J. L. (1999) Mechanisms of induction and expression of long-term depression at GABAergic synapses in the neonatal rat hippocampus. J. Neurosci. 19(17), 7568-7577.
128. Caillard, O., Ben-Ari, Y., and Gaiarsa, J. L. (1999) Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus. J. Physiol. (Lond.) 518(Pt 1), 109-119.
129. Kano, M. (1995) Plasticity of inhibitory synapses in the brain: A possible memory mechanism that has been overlooked. Neurosci. Res. 21(3), 177-182.
130. Lu, Y. M., Mansuy, I. M., Kandel, E. R., and Roder, J. (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26(1), 197-205.
131. Luscher, C. and Frerking, M. (2001) Restless AMPA receptors: Implications for synaptic transmission and plasticity. Trends Neurosci. 24(11), 665-670.
132. Hyman, S. E. and Malenka, R. C. (2001) Addiction and the brain: The neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2(10), 695-703.