Formation and plasticity of GABAergic synapses: Physiological mechanisms and pathophysiological implications

Pharmacology and Therapeutics

Volumn 98, Issue 3, 2003, Pages 299-323

  Fritschy, Jean Marc ^a   Brünig, Ina ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Benzodiazepine; GABAA receptor; Gephyrin; Neurosteroid; Synaptic clustering; Temporal lobe epilepsy

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID DERIVATIVE; ALCOHOL; ANCHORING PROTEIN RECEPTOR FOR ACTIVATED C KINASE; CELL SURFACE RECEPTOR; DOPAMINE 5 RECEPTOR; DYSTROPHIN; GAMMA AMINOBUTYRIC ACID A RECEPTOR ASSOCIATED MEMBRANE PROTEIN; GAMMA AMINOBUTYRIC ACID A RECEPTOR ASSOCIATED PROTEIN; GAMMA AMINOBUTYRIC ACID RECEPTOR INTERACTING FACTOR 1; GEPHYRIN; MUSCIMOL; NEUROSTEROID; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN KINASE C; PROTEIN SERINE KINASE; UBIQUITIN; UBIQUITIN RELATED PROTEIN 1; UNCLASSIFIED DRUG;

DRUG MECHANISM; DRUG SELECTIVITY; DRUG TARGETING; EXPERIMENTAL TEST; GABAERGIC SYSTEM; HORMONE ACTION; HUMAN; MOLECULAR DYNAMICS; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SCORING SYSTEM; SYNAPTIC TRANSMISSION; SYSTEMIC CIRCULATION;

EID: 0038362175     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0163-7258(03)00037-8     Document Type: Review

References (242)

1. A receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential. J Biol Chem. 276:2001;38934-38939.
2. A receptors uncouples allosteric binding: studies on possible mechanisms. J Neurochem. 79:2001;1100-1108.
3. Allison D.W., Gelfand V.I., Spector I., Craig A.M. Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci. 18:1998;2423-2436.
4. André V., Marescaux C., Nehlig A., Fritschy J.M. Alterations of hippocampal GABAergic system contribute to development of spontaneous recurrent seizures in the rat lithium-pilocarpine model of temporal lobe epilepsy. Hippocampus. 11:2001;452-468.
5. Baer K., Essrich C., Benson J.A., Benke D., Bluethmann H., Fritschy J.M., Luscher B. Postsynaptic clustering of γ-aminobutyric acid type A receptors by the γ3 subunit in vivo. Proc Natl Acad Sci USA. 96:1999;12860-12865.
6. A receptors in rat cerebellar granule cells by protein tyrosine kinases and protein kinase C. Biochim Biophys Acta. 1564:2002;263-270.
7. Barbaccia M.L., Affricano D., Trabucchi M., Purdy R.H., Colombo G., Agabio R., Gessa G.L. Ethanol markedly increases "GABAergic" neurosteroids in alcohol-preferring rats. Eur J Pharmacol. 384:1999;R1-R2.
8. Barbaccia M.L., Serra M., Purdy R.H., Biggio G. Stress and neuroactive steroids. Int Rev Neurobiol. 46:2001;243-272.
9. A receptors. Mohler H. Pharmacology of GABA and Glycine Neurotransmission, Vol. 150. Handbook of Pharmacology. 2001;79-100 Springer-Verlag, Berlin.
10. A receptors: classification on the basis of subunit structure and function. Pharmacol Rev. 50:1998;291-313.
11. A receptors. Int Rev Neurobiol. 48:2001;1-29.
12. A receptor polypeptides from the neuronal surface. J Protein Chem. 13:1994;437-438.
13. A receptor dysfunction in epilepsy: a mutation in the γ2-subunit gene. Nat Genet. 28:2001;46-48.
14. Baumann S.W., Baur R., Sigel E. Subunit arrangement of γ-aminobutyric acid type A receptors. J Biol Chem. 276:2001;36275-36280.
15. A receptor-associated protein, GRIF-1. J Biol Chem. 277:2002;30079-30090.
16. A receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci. 4:2001;908-916.
17. Benes F.M., Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology. 25:2001;1-27.
18. A receptors rendered diazepam-insensitive by point-mutated α-subunits. FEBS Lett. 431:1998;400-404.
19. A receptor mutations linked to epilepsy in humans. J Neurosci. 22:2002;5321-5327.
20. Biederer T., Sara Y., Mozhayeva M., Atasoy D., Liu X., Kavalali E.T., Südhof T.C. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science. 297:2002;1525-1531.
21. Blum B.P., Mann J.J. The GABAergic system in schizophrenia. Int J Neuropsychopharm. 5:2002;159-179.
22. Borden L.A. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int. 29:1996;335-356.
23. Borgdorff A.J., Choquet D. Regulation of AMPA receptor lateral movements. Nature. 417:2002;649-653.
24. Bormann J. The "ABC" of GABA receptors. Trends Pharmacol Sci. 21:2000;16-19.
25. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: EEG, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience. 89:1999;717-729.
26. A-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus. 10:2000;305-324.
27. B receptors: structure and function. Pharmacol Rev. 54:2002;247-264.
28. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem. 49:2000;38856-38862.
29. A receptor γ2 subunit in rat brain. Neuropharmacology. 41:2001;745-752.
30. A receptor function and cell surface expression. Pharmacol Ther. 94:2002;113-122.
31. A receptors with the activation of G-protein-coupled receptors. J Neurosci. 22:2002;6353-6361.
32. A receptor changes. J Chem Neuroanat. 17:1999;75-97.
33. A receptors. J Physiol. 497:1996;753-759.
34. Brickley S.G., Revilla V., Cull-Candy S.G., Wisden W., Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature. 409:2001;88-92.
35. A receptor subunit expression and function in temporal lobe epilepsy. Nat Med. 4:1998;1166-1172.
36. A receptor surface expression. Eur J Neurosci. 13:2001;1320-1328.
37. Brünig I., Scotti E., Sidler C., Fritschy J.M. Intact sorting, targeting, and clustering of γ-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol. 443:2002;43-45.
38. A receptors and gephyrin. J Neurosci. 22:2002;4805-4813.
39. A-receptor function in the adult brain: insights from the oxytocin neurone. Trends Neurosci. 23:2000;190-195.
40. A receptor subunit expression. Neuron. 19:1997;1103-1114.
41. Brussaard A.B., Wossink J., Lodder J.C., Kits K.S. Progesterone-metabolite prevents protein kinase C-dependent modulation of γ-aminobutyric acid type A receptors in oxytocin neurons. Proc Natl Acad Sci USA. 97:2000;3625-3630.
42. A receptor isoforms containing the α5 subunit subtype. Mol Pharmacol. 50:1996;119-127.
43. Carroll R., Beattie E., Xia H., Lüscher C., Altschuler Y., Nicoll R., Malenka R., von Zastrow M. Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci USA. 96:1999;14112-14117.
44. Cherubini E., Conti F. Generating diversity at GABAergic synapses. Trends Neurosci. 24:2001;155-162.
45. A receptor clustering in cultured hippocampal neurons. J Neurosci. 22:2002;684-697.
46. A receptors in HEK 293 cells. Biochemistry. 40:2001;14030-14036.
47. A receptor-ion channels. J Med Chem. 45:2002;1887-1900.
48. A receptor. J Neurosci. 22:2002;5572-5580.
49. Concas A., Mostallino M.C., Porcu P., Follesa P., Barbaccia M.L., Trabucci M., Purdy R.H., Grisenti P., Biggio G. Role of brain allopregnanolone in the plasticity of γ-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci USA. 95:1998;13284-13289.
50. Connolly C.N., Kittler J.T., Thomas P., Uren J.M., Brandon N.J., Smart T.G., Moss S.J. Cell surface stability of γ-aminobutyric acid type A receptors: dependence on protein kinase C activity and subunit composition. J Biol Chem. 51:1999;36565-36572.
51. Connolly C.N., Uren J.M., Thomas P., Gorrie G.H., Gibson A., Smart T.G., Moss S.J. Subcellular localization and endocytosis of homomeric γ2 subunit splice variants of γ-aminobutyric acid type A receptors. Mol Cell Neurosci. 13:1999;259-271.
52. A IPSCs during development in rat hippocampal or cerebellar slices. J Physiol. 521:1999;437-449.
53. Cossette P., Liu L., Brisebois K., Dong H., Lortie A., Vanasse M., Saint-Hilaire J.M., Carmant L., Verner A., Lu W.Y., Wang Y.T., Rouleau G.A. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat Genet. 31:2002;184-189.
54. Coulter D.A. Epilepsy-associated plasticity in γ-aminobutyric acid receptor expression, function, and inhibitory synaptic properties. Int Rev Neurobiol. 45:2001;237-252.
55. Craig A.M., Boudin H. Molecular heterogeneity of central synapses: afferent and target regulation. Nat Neurosci. 4:2001;569-578.
56. 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. 16:1996;3166-3177.
57. A receptors. Proc Natl Acad Sci USA. 99:2002;8980-8985.
58. A-gated currents from dissociated substantia nigra reticulata neurons. J Pharmacol Exp Ther. 291:1999;1054-1059.
59. 123I-iomazenil SPECT in presurgical evaluation of temporal lobe epilepsy? J Neurol. 62:1997;141-150.
60. A receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J Neurosci. 18:1998;8505-8514.
61. A receptors to neuroactive steroids in rats during ethanol withdrawal. J Pharmacol Exp Ther. 278:1996;510-517.
62. A receptors in the inferior olivary nucleus. J Neurophysiol. 85:2001;1686-1696.
63. Dilger J.P. The effects of general anaesthetics on ligand-gated ion channels. Br J Anaesth. 89:2002;41-51.
64. Dumoulin A., Rostaing P., Bedet C., Levi S., Isambert M.F., Henry J.P., Triller A., Gasnier B. Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci. 112:1999;811-823.
65. Duncan J.S. Positron emission tomography receptor studies in epilepsy. Rev Neurol. 155:1999;482-488.
66. Erlander M.G., Tillakaratne N.J.K., Feldblum S., Patel N., Tobin A.J. Two genes encode distinct glutamate decarboxylases. Neuron. 7:1991;91-100.
67. Esclapez M., Tillakaratne N.J.K., Kaufman D.L., Tobin A.J., Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci. 14:1994;1834-1855.
68. A receptor subtypes requires the γ2 subunit and gephyrin. Nat Neurosci. 1:1998;563-571.
69. 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. 274:1999;10100-10104.
70. A-benzodiazepine receptors in the basal ganglia in Huntington's disease and in the quinolinic acid-lesioned rat. Prog Brain Res. 99:1993;105-123.
71. A receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons. J Neurosci. 21:2001;6502-6511.
72. Ferguson S.S. Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev. 53:2001;1-24.
73. Ferns M., Carbonetto S. Challenging the neurocentric view of neuromuscular synapse formation. Neuron. 30:2001;311-314.
74. C receptors by protein kinase C. Mol Pharmacol. 57:2000;847-856.
75. Fischer F., Kneussel M., Tintrup H., Haverkamp S., Rauen T., Betz H., Wässle H. Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J Comp Neurol. 427:2000;634-648.
76. A receptors containing γ2 or δ subtypes expressed with α1 and β3 subtypes in mouse L929 cells. J Physiol. 505:1997;283-297.
77. A receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res Rev. 37:2001;81-90.
78. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;345-470.
79. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol. 359:1995;154-194.
80. A-receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol. 390:1998;194-210.
81. A-receptors in temporal lobe epilepsy. Neurochem Int. 34:1999;435-445.
82. Fuhrmann J.C., Kins S., Rostaing P., El Far O., Kirsch J., Sheng M., Triller A., Betz H., Kneussel M. Gephyrin interacts with dynein light chains 1 and 2, components of motor protein complexes. J Neurosci. 22:2002;5393-5402.
83. A receptor subunits in the substantia nigra of the rat: effects of quinolinic acid lesions of the striatum. Eur J Neurosci. 15:2002;1961-1975.
84. Gally C., Bessereau J.L. GABA is not required for differentiation of post-synaptic domains at GABAergic synapses in C. elegans. 3rd Forum of European Neuroscience, Paris, France, July 13-17, 2002, Program No. 006.2, Abstract CD-ROM:2002.
85. A-receptor subtypes: differential associations of the α1- and α3-subunits with serotonergic and GABAergic neurons. Neuroscience. 54:1993;881-892.
86. A receptor aggregates in the deep cerebellar nuclei of normal and mutant mice. J Comp Neurol. 447:2002;210-217.
87. Gasnier B. The loading of neurotransmitters into synaptic vesicles. Biochimie. 82:2000;327-337.
88. Giustetto M., Kirsch J., Fritschy J.M., Cantino D., Sassoè-Pognetto M. Localisation of the clustering protein gephyrin at GABAergic synapses in the main olfactory bulb of the rat. J Comp Neurol. 395:1998;231-244.
89. Goda Y. Cadherins communicate structural plasticity of presynaptic and postsynaptic terminals. Neuron. 35:2002;1-3.
90. Grady R.M., Zhou H., Cunningham J.M., Henry M.D., Campbell K.P., Sanes J.R. Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron. 25:2000;279-293.
91. 36Cl-flux across development in rat cerebral cortex. Dev Brain Res. 131:2001;31-39.
92. A receptors in the acute and chronic effects of ethanol. Psychopharmacology. 139:1998;2-19.
93. Hagemann G., Redecker C., Witte O.W. Intact functional inhibition in the surround of experimentally induced focal cortical dysplasias in rats. J Neurophysiol. 84:2000;600-603.
94. Henneberger C., Juttner R., Rothe T., Grantyn R. Postsynaptic action of BDNF on GABAergic synaptic transmission in the superficial layers of the mouse superior colliculus. J Neurophysiol. 88:2002;595-603.
95. Huntsmann M.M., Porcello D.M., Homanics G.E., DeLorey T.M., Huguenard J.R. Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science. 283:1999;541-543.
96. Husi H., Ward M.A., Choudhary J.S., Blackstock W.P., Grant S.G.N. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci. 3:2000;661-669.
97. A receptor desensitization kinetics and its role in synapse function in rat cortical neurons. J Physiol. 522:2000;3-17.
98. A receptor α6 subunit gene inactivation inhibits δ subunit expression. J Neurosci. 17:1997;1350-1362.
99. A receptor phosphorylation and function by neurotrophins. Soc Neurosci Abstr. 27:2001;503.07.
100. Jüttner R., Meier J., Grantyn R. Slow IPSC kinetics, low levels of α1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur J Neurosci. 13:2001;2088-2098.
101. Kananura C., Haug K., Sander T., Runge U., Gu W., Hallmann K., Rebstock J., Heils A., Steinlein O.K. A splice-site mutation in GABRG2 associated with childhood absence epilepsy and febrile convulsions. Arch Neurol. 59:2002;1137-1141.
102. A receptor function. Embo J. 21:2002;1004-1011.
103. A receptors. J Biol Chem. 274:1999;21257-21264.
104. A receptors on cultured hippocampal cells correlate only partially with functional synapses. Eur J Neurosci. 11:1999;1256-1264.
105. Katona I., Sperlágh B., Sík A., Käfalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci. 19:1999;4544-4558.
106. Katona I., Rancz E.A., Acsady L., Ledent C., Mackie K., Hajos N., Freund T.F. Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci. 21:2001;9506-9518.
107. A receptor-interacting protein. Program No. 434.4. 2002 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. CD-ROM.
108. Kins S., Betz H., Kirsch J. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nature Neurosci. 3:2000;22-29.
109. Kirischuk S., Clements J.D., Grantyn R. Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons in rat collicular cultures. J Physiol. 543:2002;99-116.
110. Kirsch J. Assembly of signaling machinery at the postsynaptic membrane. Curr Opin Neurobiol. 9:1999;329-335.
111. Kirsch J., Betz H. Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature. 392:1998;717-720.
112. Kittler J.T., Moss S.J. Neurotransmitter receptor trafficking and the regulation of synaptic strength. Traffic. 2:2001;437-448.
113. A receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci. 20:2000;7972-7977.
114. A receptors. Mol Cell Neurosci. 18:2001;13-25.
115. A receptor assembly and stoichiometry. J Neurosci. 21:2001;9124-9133.
116. A receptors in the hippocampus. J Neurosci. 22:2002;2513-2521.
117. A receptors at synaptic sites. Brain Res Rev. 39:2002;74-83.
118. Kneussel M., Betz H. Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J Physiol. 525:2000;1-9.
119. A receptor clustering in gephyrin-deficient mice. J Neurosci. 19:1999;9289-9297.
120. A R)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci USA. 97:2000;8594-8599.
121. A receptor subtypes. Mol Cell Neurosci. 17:2001;973-982.
122. A receptors. Recept Channels. 7:2000;213-226.
123. Knoll B., Drescher U. Ephrin-As as receptors in topographic projections. Trends Neurosci. 25:2002;145-149.
124. A-receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci. 11:1999;4457-4462.
125. Knuesel I., Züllig R.A., Bornhauser B., Schaub M.C., Fritschy J.M. Differential expression of utrophin and dystrophin in CNS neurons: an in situ hybridization and immunohistochemical study. J Comp Neurol. 422:2000;594-611.
126. Knuesel I., Zuellig R.A., Schaub M.C., Fritschy J.M. Alterations in dystrophin and utrophin expression parallel the reorganization of GABAergic synapses in a mouse model of temporal lobe epilepsy. Eur J Neurosci. 13:2001;1113-1124.
127. A receptor δ subunit-deficient mice: recruitment of γ2 subunits. Neuroscience. 109:2002;733-743.
128. A and glycine receptors in the mammalian retina. J Neurosci. 16:1996;2127-2140.
129. A receptors. Alcohol Clin Exp Res. 26:2002;15A.
130. A receptors containing α1 and α4 subunits in the cerebral cortex: selective effects of chronic ethanol consumption. J Neurochem. 82:2002;110-117.
131. 11C]flumazenil uptake measured using positron. Ann Neurol. 47:2000;644-648.
132. A receptors by endogenous and synthetic neuroactive steroids. Brain Res Rev. 37:2001;68-80.
133. Levi S., Vannier C., Triller A. Strychnine-sensitive stabilization of postsynaptic glycine receptor clusters. J Cell Sci. 111:1998;335-345.
134. A receptors and gephyrin expression in cultured neurons. J Neurosci. 19:1999;7434-7449.
135. Levi S., Grady M., Henry M., Campbell K., Sanes J., Craig A. Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci. 22:2002;4274-4285.
136. Lewis D.A. GABAergic local circuit neurons and prefrontal cortical dysfunction in schizophrenia. Brain Res Rev. 31:2000;270-276.
137. Lim R., Alvarez F.J., Walmsley B. Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J Physiol. 516:1999;505-512.
138. Lin J., Ju W., Foster K., Lee S., Ahmadian G., Wyszynski M., Wang Y., Sheng M. Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci. 3:2000;1282-1290.
139. Liu F., Wan Q., Pristupa Z.B., Yu X.-M., Wang Y.T., Niznik H.B. Direct protein-protein coupling enables cross-talk between dopamine D5 and γ-aminobutyric acid A receptors. Nature. 403:2000;274-280.
140. Llano I., Leresche N., Marty A. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron. 6:1991;565-574.
141. A receptor subtypes in human temporal lobe epilepsy. J Neurosci. 20:2000;5401-5419.
142. Löw K., Crestani F., Keist R., Benke D., Brünig I., Benson J.A., Fritschy J.M., Rulicke T., Bluethmann H., Mohler H., Rudolph U. Molecular and neuronal substrate for the selective attenuation of anxiety. Science. 290:2000;131-134.
143. Luhmann H.J. Ischemia and lesion induced imbalances in cortical function. Prog Neurobiol. 48:1996;131-166.
144. A receptors and associated proteins. Int Rev Neurobiol. 48:2001;31-64.
145. Malizia A.L. What do brain imaging studies tell us about anxiety disorders? J Psychopharmacol. 13:1999;372-378.
146. Mangin J.M., Guyon A., Eugene D., Paupardin-Tritsch D., Legendre P. Functional glycine receptor maturation in the absence of glycinergic input in dopaminergic neurones of the rat substantia nigra. J Physiol. 542:2002;685-697.
147. A receptor α1 subtype. Nat Neurosci. 3:2000;587-592.
148. Meier J., Vannier C., Serge A., Triller A., Choquet D. Fast and reversible trapping of surface glycine receptors by gephyrin. Nat Neurosci. 4:2001;253-260.
149. Meier J., Juttner R., Kirischuk S., Grantyn R. Synaptic anchoring of glycine receptors in developing collicular neurons under control of metabotropic glutamate receptor activity. Mol Cel Neurosci. 21:2002;324-340.
150. Meyer G., Kirsch J., Betz H., Langosch D. Identification of a gephyrin binding motif on the glycine receptor β subunit. Neuron. 15:1995;563-572.
151. Mihalek R.M., Banerjee P.K., Korpi E.R., Quinlan J.J. Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor δ subunit knockout mice. Proc Natl Acad Sci USA. 96:1999;12905-12910.
152. A receptor δ subunit knockout
153. A-receptors: pharmacology and pathophysiology. Mohler H. Pharmacology of GABA and Glycine Neurotransmission, Vol. 150. Handbook of Pharmacology. 2000;101-116 Springer-Verlag, Berlin.
154. A-receptors: from subunits to diverse functions. Narahashi T. Ion Channels, Vol. 4. 1996;89-113 Plenum Press, New York.
155. Mohler H., Fritschy J.M., Rudolph U. A new benzodiazepine pharmacology. J Pharm Exp Ther. 300:2002;2-8.
156. Morrow A.L., Van Doren M.J., Penland S.N., Matthews D.B. The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res Rev. 37:2001;98-109.
157. Moss S., Smart T. Constructing inhibitory synapses. Nat Rev Neurosci. 2:2001;240-250.
158. Nusser Z., Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol. 87:2002;2624-2628.
159. Nusser Z., Mulvihill E., Streit P., Somogyi P. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience. 61:1994;421-427.
160. Nusser Z., Sieghart W., Benke D., Fritschy J.M., Somogyi P. Differential synaptic localization of two major γ-aminobutyric acid type A receptor α subunits on hippocampal pyramidal neurons. Proc Natl Acad Sci USA. 93:1996;11939-11944.
161. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J Neurosci. 16:1996;103-114.
162. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci. 18:1998;1693-1703.
163. A-benzodiazepine receptor in psychiatric disorder. Br J Psychiatry. 179:2001;390-396.
164. A receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci. 13:2001;428-442.
165. A receptors. J Neurochem. 80:2002;815-823.
166. Okazaki N., Yan J., Yuasa S., Ueno T., Kominami E., Masuho Y., Koga H., Muramatsu M. 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. Mol Brain Res. 85:2000;1-12.
167. Olsen R.W., DeLorey T.M., Gordey M., Kang M.H. GABA receptor function and epilepsy. Adv Neurol. 79:1999;499-510.
168. A receptors: regulation by corticosterone. J Neurosci. 21:2001;330-339.
169. Pawelzik H., Hughes D.I., Thomson A.M. Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol. 443:2002;346-367.
170. A receptor changes in δ subunit-deficient mice: altered expression of α4 and γ2 subunits in the forebrain. J Comp Neurol. 446:2002;179-197.
171. Pfeiffer F., Simler R., Grenningloh G., Betz H. Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc Natl Acad Sci USA. 81:1984;7224-7227.
172. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience. 101:2000;815-850.
173. A responses in hippocampal pyramidal cells. J Neurosci. 12:1992;4122-4132.
174. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science. 293:2001;1159-1163.
175. Quick M.W., Corey J.L., Davidson N., Lester H.A. Second messengers, trafficking-related proteins, and amino acid residues that contribute to the functional regulation of the rat brain GABA transporter GAT1. J Neurosci. 17:1997;2967-2979.
176. Rao A., Cha E.M., Craig A.M. Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci. 20:2000;8344-8353.
177. Rao A., Harms K.J., Craig A.M. Neuroligation: building synapses around the neurexin-neuroligin link. Nat Neurosci. 3:2000;747-749.
178. A receptor function and seizure susceptibility. J Neurosci. 22:2002;3795-3805.
179. Redecker C., Lutzenburg M., Gressens P., Evrard P., Witte O.W., Hagemann G. Excitability changes and glucose metabolism in experimentally induced focal cortical dysplasias. Cerebral Cortex. 8:1998;623-834.
180. A receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J Neurosci. 20:2000;5045-5053.
181. A-receptor subtypes after focal cortical infarcts in rats: mediation by NMDA-dependent processes. J Cereb Blood Flow Metab. 22:2002;1463-1475.
182. Riban V., Bouilleret V., Pham-Lè B.T., Fritschy J.M., Marescaux C., Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience. 112:2002;101-111.
183. Rosenberg M., Meier J., Triller A., Vannier C. Dynamics of glycine receptor insertion in the neuronal plasma membrane. J Neurosci. 21:2001;5036-5044.
184. A receptor subtypes. Nature. 401:1999;796-800.
185. A receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci. 22:2001;188-194.
186. Sabatini D.M., Barrow R.K., Blackshaw S., Burnett P.E., Lai M.M., Field M.E., Bahr B.A., Kirsch J., Betz H., Snyder S.H. Interaction of RAFT1 with gephyrin required for rapamycin-sensitive signaling. Science. 284:1999;1161-1164.
187. Sanes J.R., Lichtman J.W. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci. 2:2001;791-805.
188. A-receptor subunits in the rat retina. J Comp Neurol. 357:1995;1-14.
189. A receptor subtypes with gephyrin at postsynaptic sites. J Comp Neurol. 420:2000;481-498.
190. Savic I., Roland P., Sedvall G., Persson A., Pauli S., Widen L. In vivo demonstration of reduced benzodiazepine receptor binding in human epileptic foci. Lancet. ii:1988;863-866.
191. A receptor subunits: role of the δ subunit. J Neurosci. 14:1994;7077-7086.
192. A receptor β subunits and the multifunctional protein gC1q-R. J Biol Chem. 276:2001;26597-26604.
193. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell. 101:2000;657-669.
194. A receptor subunits in the rat hippocampus. II. Altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience. 80:1997;1001-1017.
195. A receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J Comp Neurol. 433:2001;526-549.
196. Scotti A.L., Reuter H. Synaptic and extrasynaptic γ-aminobutyric acid type A receptor clusters in rat hippocampal cultures during development. Proc Natl Acad Sci USA. 98:2001;3489-3494.
197. A receptor function in rat brain. J Neurochem. 75:2000;732-740.
198. Sheng M., Lee S. AMPA receptor trafficking and the control of synaptic transmission. Cell. 105:2001;825-828.
199. Sheng M., Sala C. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci. 24:2001;1-29.
200. A receptor subtypes. Pharmacol Rev. 47:1995;181-234.
201. A receptor subtypes. Trends Pharmacol Sci. 21:2000;411-413.
202. A receptors. Neurochem Int. 34:1999;379-385.
203. A receptors. Drugs Future. 26:2001;1191-1197.
204. A receptor subunits in the dentate gyrus of the rat and cell type-specific up-regulation following entorhinal cortex lesion. Neuroscience. 102:2001;789-803.
205. A receptor gene regulation in the brain and anxiety behavior. Steroids. 67:2002;519-528.
206. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature. 392:1998;926-930.
207. Soghomonian J.J., Martin D.L. Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci. 19:1998;500-505.
208. Song J.Y., Ichtchenko K., Sudhof T.C., Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA. 96:1999;1100-1105.
209. A receptor δ subunit. Epilepsia. 43:2002;3-8.
210. A conductances in hippocampal neurons. J Neurosci. 22:2002;1-5.
211. Studler B., Fritschy J.M., Brünig I. GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro. Neuroscience. 114:2002;123-133.
212. A receptors are a target for alcohol. Nat Neurosci. 5:2002;721-722.
213. A synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci. 17:1997;2959-2966.
214. A/benzodiazepine receptors in chick cortical neurons. J Neurochem. 57:1991;1307-1312.
215. Tietz E.I., Zeng X.J., Chen S., Lilly S.M., Rosenberg H.C., Kometiani P. Antagonist-induced reversal of functional and structural measures of hippocampal benzodiazepine tolerance. J Pharmacol Exp Ther. 291:1999;932-942.
216. Treimann D. GABAergic mechanisms in epilepsy. Epilepsia. 42:2001;8-12.
217. A receptor δ subunit gene leads to an up-regulation of γ2 subunit-containing receptors in cerebellar granule cells. J Biol Chem. 276:2001;10532-10538.
218. Triller A., Cluzeaud F., Pfeiffer F., Betz H., Korn H. Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J Cell Biol. 101:1985;683-688.
219. Tsao P.I., von Zastrow M. Diversity and specificity in the regulated endocytic membrane trafficking of G-protein-coupled receptors. Pharmacol Ther. 89:2001;139-147.
220. Turrigiano G.G. AMPA receptors unbound: membrane cycling and synaptic plasticity. Neuron. 26:2000;5-8.
221. Unwin N. Neurotransmitter action: opening of a ligand-gated channel. Neuron. 10(suppl.):1993;31-41.
222. van Zundert B., Alvarez F.J., Yevenes G.E., Carcamo J.G., Vera J.C., Aguayo L.G. Glycine receptors involved in synaptic transmission are selectively regulated by the cytoskeleton in mouse spinal neurons. J Neurophysiol. 87:2002;640-644.
223. Vautrin J., Maric D., Sukhareva M., Schaffner A.E., Barker J.L. Surface-accessible GABA supports tonic and quantal synaptic transmission. Synapse. 37:2000;38-55.
224. A receptors depend upon subunit composition. Neuron. 4:1990;919-928.
225. A receptor α1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci. 21:2001;3009-3016.
226. A receptor α2 subunit in the prefrontal cortex in schizophrenia. Cerebral Cortex. 12:2002;1063-1070.
227. A receptors in the primate basal ganglia: an autoradiographic and a light and electron microscopic immunohistochemical study of the α1 and β2,3 subunits in the baboon brain. J Comp Neurol. 397:1998;297-325.
228. Walikonis R.S., Jensen O.N., Mann M., Provance D.W., Mercer J.A., Kennedy M.B. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J Neurosci. 20:2000;4069-4080.
229. A receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci. 9:1997;533-548.
230. A receptor γ2-subunit in childhood absence epilepsy and febrile seizures. Nat Gen. 28:2001;49-52.
231. A receptors to postsynaptic domains by insulin. Nature. 388:1997;686-690.
232. A receptors and the cytoskeleton. Nature. 397:1999;69-72.
233. A receptor gene family: new targets for therapeutic intervention. Neurochem Int. 34:1999;387-390.
234. Wilkinson D.G. Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci. 2:2001;155-164.
235. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science. 296:2002;678-682.
236. Wilson R.I., Kunos G., Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron. 31:2001;453-462.
237. Wingrove P.B., Safo P., Wheat L., Thompson S.A., Wafford K.A., Whiting P.J. Mechanism of α-subunit selectivity of benzodiazepine pharmacology at γ-aminobutyric acid type A receptors. Eur J Neurosci. 437:2002;31-39.
238. A receptor α6 subunit in hippocampal pyramidal neurons produces extrasynaptic receptors and an increased tonic inhibition. Neuropharmacology. 43:2002;530-549.
239. A receptors containing the δ subunit. J Neurosci. 22:2002;1541-1549.
240. Woo T.U., Whitehead R.E., Melchitzky D.S., Lewis D.A. A subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci USA. 95:1998;5341-5346.
241. Yamagata M., Weiner J.A., Sanes J.R. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell. 110:2002;649-660.
242. Zinder O., Dar D.E. Neuroactive steroids; their mechanism of action and their function in the stress response. Acta Physiol Scand. 167:1999;181-188.