Ethanol regulation of γ-aminobutyric acidA receptors: Genomic and nongenomic mechanisms

Pharmacology and Therapeutics

Volumn 101, Issue 3, 2004, Pages 211-226

  Kumar, Sandeep ^a   Fleming, Rebekah L ^a   Morrow, A Leslie ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

A kinase anchoring proteins; Adaptor complex 2; AKAP; AP2; BDNF; Brain derived neurotrophic factor; CaMK; GABAA receptor expression; Neurosteroids; Protein kinase C; Receptor phosphorylation; Subcellular localization; Synaptic localization

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL;

ALCOHOL TOLERANCE; ALCOHOLISM; CELLULAR DISTRIBUTION; GENE EXPRESSION; GENOMICS; HUMAN; MOTOR COORDINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REINFORCEMENT; REVIEW; RNA TRANSLATION; SEDATION; SIGNAL TRANSDUCTION; TRANQUILIZING ACTIVITY;

ALCOHOLISM; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DRUG TOLERANCE; ETHANOL; HUMANS; RECEPTORS, GABA-A;

EID: 1542718638     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2003.12.001     Document Type: Review

References (163)

1. Aguayo L.G., Pancetti F.C., Klein R.L., Harris R.A. Differential effects of GABAergic ligands in mouse and rat hippocampal neurons. Brain Res. 647:1994;97-105.
2. Allan A.M., Harris R.A. Acute and chronic ethanol treatments alter GABA receptor-operated chloride channels. Pharmacol Biochem Behav. 27:1987;665-670.
3. Bao J., Alroy I., Waterman H., Schejter E.D., Brodie C., Gruenberg J., Yarden Y. Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J Biol Chem. 275:2000;26178-26186.
4. 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.
5. Barmack N.H., Qian Z., Yoshimura J. Regional and cellular distribution of protein kinase C in rat cerebellar Purkinje cells. J Comp Neurol. 427:2000;235-254.
6. Bencsits E., Ebert V., Tretter V., Sieghart W. A significant part of native gamma-aminobutyric acidA receptors containing alpha4 subunits do not contain gamma or delta subunits. J Biol Chem. 274:1999;19613-19616.
7. Boisse N.N., Okamoto M. Ethanol as a sedative-hypnotic: comparison with barbiturate and non-barbiturate sedative-hypnotics. Rigter H., Crabbe J.C. Alcohol Tolerance and Dependence. 1980;265-292 Elsevier, Amsterdam.
8. Bowers B.J., Elliott K.J., Wehner J.M. Differential sensitivity to the anxiolytic effects of ethanol and flunitrazepam in PKCgamma null mutant mice. Pharmacol Biochem Behav. 69:2001;99-110.
9. Brandon N.J., Uren J.M., Kittler J.T., Wang H., Olsen R., Parker P.J., Moss S.J. Subunit specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci. 19:1999;9228-9234.
10. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem. 275:2000;38856-38862.
11. Brandon N.J., Jovanovic J.N., Smart T.G., Moss S.J. Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors. J Neurosci. 22:2002;6353-6361.
12. Brandon N.J., Jovanovic J.N., Colledge M., Kittler J.T., Brandon J.M., Scott J.D., Moss S.J. A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor beta subunits. Mol Cell Neurosci. 22:2003;87-97.
13. Brown M.E., Anton R.F., Malcolm R., Ballenger J.C. Alcohol detoxification and withdrawal seizures: clinical support for a kindling hypothesis. Biol Psychiatry. 23:1988;507-514.
14. A receptor surface expression. Eur J Neurosci. 13:2001;1320-1328.
15. Buchner K., Adamec E., Beermann M.L., Nixon R.A. Isoform-specific translocation of protein kinase C following glutamate administration in primary hippocampal neurons. Brain Res Mol Brain Res. 64:1999;222-235.
16. A receptor-operated chloride channels: II. Chronic effects of ethanol. J Pharmacol Exp Ther. 253:1990;713-719.
17. A receptors. Mol Pharmacol. 63:2003;53-64.
18. Celentano J.J., Gibbs T.T., Farb D.H. Ethanol potentiates GABA- and glycine-induced chloride currents in chick spinal cord neurons. Brain Res. 455:1988;377-380.
19. Chapell R., Bueno O.F., Alvarez-Hernandez X., Robinson L.C., Leidenheimer N.J. Activation of protein kinase C induces gamma-aminobutyric acid type A receptor internalization in Xenopus oocytes. J Biol Chem. 273:1998;32595-32601.
20. A receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci USA. 97:2000;11557-11562.
21. Churn S.B., DeLorenzo R.J. Modulation of GABAergic receptor binding by activation of calcium and calmodulin-dependent kinase II membrane phosphorylation. Brain Res. 809:1998;68-76.
22. A receptor alpha1 subunit modulates benzodiazepine binding. J Neurochem. 82:2002;1065-1076.
23. Cinar H., Barnes E.M. Jr. Clathrin-independent endocytosis of GABA(A) receptors in HEK 293 cells. Biochemistry. 40:2001;14030-14036.
24. Connolly C.N., Kittler J.T., Thomas P., Uren J.M., Brandon N.J., Smart T.G., Moss S.J. Cell surface stability of gamma-aminobutyric acid type A receptors: dependence on protein kinase C activity and subunit composition. J Biol Chem. 274:1999;36565-36572.
25. Crews F., Morrow A.L., Criswell H., Breese G. Effects of ethanol on ion channels. Bradley R.J., Harris R.A. International Review of Neurobiology. vol. 39:1996;283-367 Academic Press, New York.
26. Criswell H.E., Simson P.E., Johnson K.B., Breese G.R. Chronic ethanol decreases the ability of GABA to inhibit ethanol-sensitive neurons in the medial septum. Alcohol Clin Exp Res. 17:1993;477.
27. Devaud L.L., Purdy R.H., Morrow A.L. The neurosteroid, 3α-hydroxy-5α-pregnan-20-one, protects against bicuculline-induced seizures during ethanol withdrawal in rats. Alcohol Clin Exp Res. 19:1995;350-355.
28. Devaud L.L., Smith F.D., Grayson D.R., Morrow A.L. Chronic ethanol consumption differentially alters the expression of γ-aminobutyric acid type A receptor subunit mRNAs in rat cerebral cortex: competitive, quantitative reverse transcriptase-polymerase chain reaction analysis. Mol Pharmacol. 48:1995;861-868.
29. A receptors to neuroactive steroids in rats during ethanol withdrawal. J Pharmacol Exp Ther. 278:1996;510-517.
30. A receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J Neurochem. 69:1997;126-130.
31. A receptors in rats. Brain Res. 796:1998;222-230.
32. Dohrman D.P., Chen H.M., Gordon A.S., Diamond I. Ethanol-induced translocation of protein kinase A occurs in two phases: control by different molecular mechanisms. Alcohol Clin Exp Res. 26:2002;407-415.
33. Dombradi V., Krieglstein J., Klumpp S. Regulating the regulators. Conference on protein phosphorylation and protein phosphatases. EMBO Rep. 3:2002;120-124.
34. Ericson M., Haythornthwaite A.R., Yeh P.W., Yeh H.H. Brain-derived neurotrophic factor mitigates chronic ethanol-induced attenuation of gamma-aminobutyric acid responses in cultured cerebellar granule cells. J Neurosci Res. 73:2003;722-730.
35. Etoh S., Baba A., Iwata H. NMDA induces protein kinase C translocation in hippocampal slices of immature rat brain. Neurosci Lett. 126:1991;119-122.
36. Fancsik A., Linn D.M., Tasker J.G. Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J Neurosci. 20:2000;3067-3075.
37. Feng J., Cai X., Zhao J., Yan Z. Serotonin receptors modulate GABA(A) receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons. J Neurosci. 21:2001;6502-6511.
38. Finn D.A., Gallaher E.J., Crabbe J.C. Differential change in neuroactive steroid sensitivity during ethanol withdrawal. J Pharmacol Exp Ther. 292:2000;394-405.
39. Flores-Hernandez J., Hernandez S., Snyder G.L., Yan Z., Fienberg A.A., Moss S.J., Greengard P., Surmeier D.J. D(1) dopamine receptor activation reduces GABA(A) receptor currents in neostriatal neurons through a PKA/DARPP-32/PP1 signaling cascade. J Neurophysiol. 83:2000;2996-3004.
40. Freund R.K., Palmer M.R. Beta adrenergic sensitization of gamma-aminobutyric acid receptors to ethanol involves a cyclic AMP/protein kinase A second-messenger mechanism. J Pharmacol Exp Ther. 280:1997;1192-1200.
41. Frye G.D., Chapin R.E., Vogel R.A., Mailman R.B., Kilts C.D., Mueller R.A., Breese G.R. Effects of acute and chronic 1,3-butanediol treatment on central nervous system function: a comparison with ethanol. J Pharmacol Exp Ther. 216:1981;306-314.
42. A antagonist-induced seizures and agonist-stimulated chloride uptake. Alcohol. 8:1993;453-459.
43. A-activated currents in adult medial septum/diagonal band neurons. Brain Res. 635:1994;283-292.
44. Gallo M.A., Smith S.S. Progesterone withdrawal decreases latency to and increases duration of electrified prod burial: a possible rat model of PMS anxiety. Pharmacol Biochem Behav. 46:1993;897-904.
45. Ghansah E., Weiss D.S. Modulation of GABA(A) receptors by benzodiazepines and barbiturates is autonomous of PKC activation. Neuropharmacology. 40:2001;327-333.
46. Givens B.S., Breese G.R. Site-specific enhancement of γ-aminobutyric acid-mediated inhibition of neural activity by ethanol in the rat medial septum. J Pharmacol Exp Ther. 254:1990;528-538.
47. Givens B.S., McMahon K. Effects of ethanol on nonspatial working memory and attention in rats. Behav Neurosci. 111:1997;275-282.
48. Gonzalez L.P., Czachura J.F. Reduced behavioral responses to intranigral muscimol following chronic ethanol. Physiol Behav. 46:1989;473-477.
49. A receptors in the acute and chronic effects of ethanol. Psychopharmacology. 139:1998;2-19.
50. A receptor subunits in rat cortex in a region-specific manner. Alcohol Clin Exp Res. 24:2000;1137-1144.
51. Harris R.A., McQuilkin S.J., Paylor R., Abeliovich A., Tonegawa S., Wehner J.M. Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered functions of gamma-aminobutyrate type A receptors. Proc Natl Acad Sci USA. 92:1995;3658-3662.
52. Harris R.A., Mihic S.J., Valenzuela C.F. Alcohol and benzodiazepines: recent mechanistic studies. Drug Alcohol Depend. 51:1998;155-164.
53. A receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the β2 subunit of the receptor. J Biol Chem. 278:2003;24046-24052.
54. Heuschneider G., Schwartz R.D. cAMP and forskolin decrease γ-aminobutyric acid-gated chloride flux in rat brain synaptoneurosomes. Proc Natl Acad Sci USA. 86:1989;2938-2942.
55. Hirst J., Robinson M.S. Clathrin and adaptors. Biochim Biophys Acta. 1404:1998;173-193.
56. A receptor modulators and alcohol in mice lacking PKCε Nat Neurosci. 2:1999;997-1002.
57. Hsu F.C., Waldeck R., Faber D.S., Smith S.S. Neurosteroid effects on GABAergic synaptic plasticity in hippocampus. J Neurophysiol. 89:2003;1929-1940.
58. Huang R.Q., Dillon G.H. Maintenance of recombinant type A gamma-aminobutyric acid receptor function: role of protein tyrosine phosphorylation and calcineurin. J Pharmacol Exp Ther. 286:1998;243-255.
59. Janis G.C., Devaud L.L., Mitsuyama H., Morrow A.L. Effects of chronic ethanol consumption and withdrawal on the neuroactive steroid 3α-hydroxy-5α-pregnan-20-one in male and female rats. Alcohol Clin Exp Res. 22:1998;2055-2061.
60. A receptor subunit protein expression via a protein kinase C-dependent mechanism. Br J Pharmacol. 124:1998;1338-1340.
61. A receptor beta3 subunit. Program Number 522.1 2000 Abstract Viewer/Itinerary Planner. 2000;Society for Neuroscience, Washington, DC.
62. A receptors to allosteric modulatory drugs in rat hippocampus after chronic intermittent ethanol treatment. Alcohol Clin Exp Res. 22:1998;2165-2173.
63. A receptors. J Biol Chem. 274:1999;21257-21264.
64. Kano M., Konnerth A. Potentiation of GABA-mediated currents by cAMP-dependent protein kinase. NeuroReport. 3:1992;563-566.
65. Kano M., Rexhausen U., Dreessen J., Konnerth A. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature. 356:1992;601-604.
66. A receptor is modulated by protein kinase C via multiple phosphorylation sites. J Biol Chem. 267:1992;25660-25663.
67. Kikkawa U., Kishimoto A., Nishizuka Y. The protein kinase C family: heterogeneity and its implications. Annu Rev Biochem. 58:1989;31-44.
68. A receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci. 20:2000;7972-7977.
69. A receptor function and binding in stably transfected cells: chronic ethanol treatment. Alcohol Clin Exp Res. 19:1995;1338-1344.
70. A receptor α1 subunit knockout mice. J Pharmacol Exp Ther. 302:2002;1037-1045.
71. A receptor α1 subunit deletion alters receptor subtype assembly, pharmacological and behavioral responses to benzodiazepines and zolpidem. Neuropharmacology. 43:2002;685-694.
72. A receptor function by protein kinase C phosphorylation. Neuron. 12:1994;1081-1095.
73. 4 subunits in the cerebral cortex: selective effects of chronic ethanol consumption. J Neurochem. 82:2002;110-117.
74. - uptake in cerebral cortical synaptoneurosomes and modulates the hypnotic effect of muscimol in rats. Program Number 569.1 2003 Abstract Viewer/Itinerary Planner. 2003;Society for Neuroscience, Washington, DC.
75. A receptors in cerebral cortex. J Neurochem. 86:2003;700-708.
76. Le A.D., Khanna J.M., Kalant H., Grossi F. Tolerance to and cross-tolerance among ethanol, pentobarbital and chlordiazepoxide. Pharmacol Biochem Behav. 24:1986;93-98.
77. A receptors. Brain Res Mol Brain Res. 52:1997;173-181.
78. A receptor complex function. Mol Pharmacol. 38:1990;823-828.
79. A receptor: role of desensitization. Mol Pharmacol. 41:1992;1116-1123.
80. A receptor whole-cell currents by protein kinase C is mediated through phosphorylation of both β1 and γ2L subunits. Mol Pharmacol. 50:1996;184-195.
81. Lodish H., Baltimore D., Berk A., Zipursky S.L., Matsuaira P., Darnell J. Synthesis and sorting of plasma membrane, secretory, and lysosomal proteins. Molecular Cell Biology. 3rd ed. 1996;711-715 Freeman, New York.
82. Macdonald R.L. Ethanol, γ-aminobutyrate type A receptors, and protein kinase C phosphorylation. Proc Natl Acad Sci USA. 92:1995;3633-3635.
83. MacLennan A.J., Lee N., Walker D.W. Chronic ethanol administration decreases brain-derived neurotrophic factor gene expression in the rat hippocampus. Neurosci Lett. 197:1995;105-108.
84. A receptor α4-subunit expression: possible relevance to alcohol dependence. J Neurochem. 68:1997;2485-2492.
85. Majchrowicz E. Induction of physical dependence upon ethanol and the associated behavioral changes. Psychopharmacologia. 43:1975;245-254.
86. Marszalec W., Aistrup G.L., Narahashi T. Ethanol modulation of excitatory and inhibitory synaptic interactions in cultured cortical neurons. Alcohol Clin Exp Res. 22(7):1998;1516-1524.
87. Martz A., Deitrich R.A., Harris R.A. Behavioral evidence for the involvement of gamma-aminobutyric acid in the actions of ethanol. Eur J Pharmacol. 89:1983;53-62.
88. Matthews D.B., Simson P.E., Best P.J. Acute ethanol impairs spatial memory but not stimulus/response memory in the rat. Alcohol Clin Exp Res. 19:1995;902-909.
89. A receptor gene expression by ethanol in the rat hippocampus vs. cerebral cortex. J Neurochem. 70:1998;1160-1166.
90. A receptor subunit peptide expression and function in the rat. Soc Neurosci Abstr. 24:1998;1831.
91. 2+/calmodulin type II-dependent protein kinase. Neuropharmacology. 36:1997;1377-1385.
92. A receptor B subunits determine regulation by cAMP- dependent protein kinase. Nature Neurosci. 1:1998;23-28.
93. Mehta A.K., Ticku M.K. Chronic ethanol treatment alters the behavioral effects of Ro 15-4513, a partially negative ligand for benzodiazepine binding sites. Brain Res. 489:1989;93-100.
94. Messing R.O., Peterson P.J., Henrich C.J. Chronic ethanol exposure increases levels of protein kinase Cδ and ε and protein kinase C-mediated phosphorylation in cultured neural cells. J Biol Chem. 266:1991;23428-23432.
95. Mhatre M.C., Ticku M.K. Chronic ethanol administration alters γ-aminobutyric acid A receptor gene expression. Mol Pharmacol. 42:1992;415-422.
96. A receptor α subunit polypeptide expression in rat cerebral cortex and cerebellum. Alcohol Clin Exp Res. 17:1993;442.
97. A and glycine receptors. Nature. 389:1997;385-389.
98. Mody I. Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochem Res. 26:2001;907-913.
99. A receptors: from subunits to diverse functions. Narahashi T. Ion Channels. vol. 4:1996;89-111 Plenum, New York.
100. Moran M.H., Smith S.S. Progesterone withdrawal I: pro-convulsant effects. Brain Res. 807:1998;84-90.
101. Moran M.H., Goldberg N., Smith S.S. Progesterone withdrawal: II. Insensitivity to the sedative effects of a benzodiazepine. Brain Res. 807:1998;91-100.
102. - uptake in cerebral cortical synaptoneurosomes. J Pharmacol Exp Ther. 246:1988;158-164.
103. A receptor α1 and α6 subunit mRNA levels in rat cerebellum. Mol Cell Neurosci. 3:1992;251-258.
104. Morrow A.L., VanDoren M.J., Devaud L.L. Effects of progesterone or neuroactive steroid? Nature. 395:1998;652-653.
105. Morrow A.L., Janis G.C., VanDoren M.J., Matthews D.B., Samson H.H., Janak P.H., Grant K.A. Neurosteroids mediate pharmacological effects of ethanol: a new mechanism of ethanol action? Alcohol Clin Exp Res. 23:1999;1933-1940.
106. A receptors in rat cortex by a PKC-dependent mechanism. ACNP 40th Annual Meeting. 2001;215 ACNP Secretariat, Waikoloa, HI.
107. Morrow A.L., VanDoren M.J., Penland S.N., Matthews D.B. The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res Brain Res Rev. 37:2001;98-109.
108. A Receptor. 2003;219-245 CRC Press, Miami, FL.
109. Moss S.J., Doherty C.A., Huganir R.L. Identification of the cAMP-dependent protein kinase and protein kinase C phosphorylation sites within the major intracellular domains of the β1, γ2S and γ2L subunits of the γ-aminobutyric acid type A receptor. J Biol Chem. 267:1992;14470-14476.
110. A receptors by cAMP-dependent protein phosphorylation. Science. 257:1992;661-665.
111. 2+-dependent protein kinase C isoforms induced by chronic ethanol treatment in mice. Neurosci Lett. 307:2001;85-88.
112. A receptors by cAMP-dependent protein kinase in mouse cerebellar and olfactory bulb neurones. J Physiol. 521(Pt 2):1999;421-435.
113. Nymann-Andersen J., Wang H., Chen L., Kittler J.T., Moss S.J., Olsen R.W. Subunit specificity and interaction domain between GABA(A) receptor-associated protein (GABARAP) and GABA(A) receptors. J Neurochem. 80:2002;815-823.
114. Obrietan K., Gao X.B., Van Den Pol A.N. Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism - a positive feedback circuit in developing neurons. J Neurophysiol. 88:2002;1005-1015.
115. A receptor binding in rat brain slices. Brain Res. 850:1999;158-165.
116. A receptor subunits in the mouse limbic system. NeuroReport. 11:2000;683-687.
117. - uptake in mesocorticolimbic regions of rat brain. Alcohol Clin Exp Res. 25:2001;1270-1275.
118. Peng Z., Hauer B., Mihalek R.M., Homanics G.E., Sieghart W., Olsen R.W., Houser C.R. GABA(A) receptor changes in delta subunit-deficient mice: altered expression of alpha4 and gamma2 subunits in the forebrain. J Comp Neurol. 446:2002;179-197.
119. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience. 101:2000;815-850.
120. A receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci. 19:1999;674-683.
121. A receptor current in mouse spinal neurons. Neuron. 5:1990;789-796.
122. A receptor-mediated responses in cerebral cortical neurons in rat brain slices. Brain Res. 595:1992;220-227.
123. A receptor-mediated responses in protein kinase C gamma (PKC gamma) and PKC epsilon null mice. J Pharmacol Exp Ther. 305:2003;264-270.
124. A receptors. Neuron. 4:1990;759-765.
125. - currents. Mol Pharmacol. 39:1991;691-696.
126. - currents in neurons of the chick, rat and mouse central nervous system. Eur J Pharmacol. 224:1992;173-181.
127. A receptor in cerebellar granule cells in culture: differential involvement of kinase activities. Neuroscience. 53:1993;131-138.
128. A receptor activity by NMDA receptor activation in rat cerebellum granule cells. Eur Biophys J. 25:1997;181-187.
129. Roberto M., Madamba S.G., Moore S.D., Tallent M.K., Siggins G.R. Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci USA. 100:2003;2053-2058.
130. Romeo E., Brancati A., De Lorenzo A., Fucci P., Furnari C., Pompili E., Sasso G.F., Spalletta G., Troisi A., Pasini A. Marked decrease of plasma neuroactive steroids during alcohol withdrawal. J Pharmacol Exp Ther. 247:1996;309-322.
131. A receptor interactions: a comparison between cell lines and cerebellar Purkinje cells. J Pharmacol Exp Ther. 284:1998;768-776.
132. Sassoe-Pognetto M., Panzanelli P., Sieghart W., Fritschy J.M. Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J Comp Neurol. 420:2000;481-498.
133. A receptor family: molecular and functional diversity. Cold Spring Harbor Symp Quant Biol. 55:1990;29-38.
134. A receptor binding, and benzodiazepine-resistant anxiety. J Neurosci. 20:2000;2758-2765.
135. A receptors. Trends Pharmacol Sci. 10:1989;407-409.
136. A receptor subtypes. Trends Pharmacol Sci. 21:2000;411-413.
137. Sieghart W., Sperk G. Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem. 2:2002;795-816.
138. A receptors. Neurochem Int. 34:1999;379-385.
139. Sik A., Gulacsi A., Lai Y., Doyle W.K., Pacia S., Mody I., Freund T.F. Localization of the A kinase anchoring protein AKAP79 in the human hippocampus. Eur J Neurosci. 12:2000;1155-1164.
140. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature. 392:1998;926-930.
141. A receptor α4 subunit in association with increased anxiety. J Neurosci. 18:1998;5275-5284.
142. A receptor-mediated chloride currents in hippocampal, cortical, and septal neurons in rat brain slices. Synapse. 18:1994;94-103.
143. A receptors are a target for alcohol. Nat Neurosci. 5:2002;721-722.
144. 2+ increase by amino acids in primary cultured rat cortical neurons. Neurochem Int. 32:1998;205-211.
145. Tapia-Arancibia L., Rage F., Givalois L., Dingeon P., Arancibia S., Beauge F. Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J Neurosci Res. 63:2001;200-208.
146. Thiele T.E., Willis B., Stadler J., Reynolds J.G., Bernstein I.L., McKnight G.S. High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J Neurosci. 20:2000;RC75.
147. A receptor desensitization in mice spinal cord cultured neurons: lack of involvement of protein kinases A and C. Mol Pharmacol. 38:1990;719-724.
148. A receptor subtype. J Neurosci. 17:1997;2728-2737.
149. Ulfig N., Setzer M. Expression of a kinase anchoring protein 79 in the human fetal amygdala. Microsc Res Tech. 46:1999;48-52.
150. VanDoren M.J., Matthews D.B., Janis G.C., Grobin A.C., Devaud L.L., Morrow A.L. Neuroactive steroid 3α-hydroxy-5α-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. J Neurosci. 20:2000;1982-1989.
151. Wafford K.A., Thompson S.A., Thomas D., Sikela J., Wilcox A.S., Whiting P.J. Functional characterization of human gamma-aminobutyric acidA receptors containing the alpha4 subunit. Mol Pharmacol. 50:1996;670-678.
152. 3δγ-aminobutyric acid type A receptors at low
153. B receptors. Proc Natl Acad Sci USA. 93:1996;5049-5054.
154. A receptor interaction. J Neurochem. 75:2000;644-655.
155. Wang Y., Freund R.K., Palmer M.R. Potentiation of ethanol effects in cerebellum by activation of endogenous noradrenergic inputs. J Pharmacol Exp Ther. 288:1999;211-220.
156. A-mediated synaptic current by ethanol in hippocampal CA1 neurons: possible role of protein kinase C. J Pharmacol Exp Ther. 268:1994;1388-1395.
157. A synapses onto rat hippocampal CA1 pyramidal neurons. J Neurophysiol. 77:1997;1306-1312.
158. A receptors in rat hippocampal CA1 pyramidal neurons. J Neurochem. 68:1997;1949-1959.
159. Wetsel W.C., Khan W.A., Merchenthaler I., Rivera H., Halpern A.E., Phung H.M., Negro-Vilar A., Hannun Y.A. Tissue and cellular distribution of the extended family of protein kinase C isoenzymes. J Cell Biol. 117:1992;121-133.
160. A alpha4 subunit expressed in Xenopus laevis oocytes. Mol Pharmacol. 50:1996;1365-1375.
161. 4 subunit. FEBS Lett. 289:1991;227-230.
162. Yoshida Y., Huang F.L., Nakabayashi H., Huang K.P. Tissue distribution and developmental expression of protein kinase C isozymes. J Biol Chem. 263:1988;9868-9873.
163. Zafra F., Castren E., Thoenen H., Lindholm D. Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc Natl Acad Sci USA. 88:1991;10037-10041.