Pharmacological and functional implications of developmentally-regulated changes in GABA(A) receptor subunit expression in the cerebellum

European Journal of Pharmacology

Volumn 352, Issue 1, 1998, Pages 1-14

  Carlson, Berit X ^a   Elster, Lisbeth ^a   Schousboe, Arne ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Benzodiazepine insensitive binding; Cerebellar granule cell; Cultured neuron; GABA ( aminobutyric acid) affinity; Neurodifferentiation; 6 subunit

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 8 AZIDO 5,6 DIHYDRO 5 METHYL 6 OXO 4H IMIDAZO[1,5 A][1,4]BENZODIAZEPINE 3 CARBOXYLIC ACID ETHYL ESTER; ANTIMITOTIC AGENT; BENZODIAZEPINE DERIVATIVE; BICUCULLINE; DIAZEPAM; FLUNITRAZEPAM; GABOXADOL; MUSCIMOL; RECEPTOR SUBTYPE;

BRAIN DEVELOPMENT; BRAIN MATURATION; CEREBELLUM; GRANULE CELL; HUMAN; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR AFFINITY; REVIEW;

EID: 0031822375     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(98)00355-0     Document Type: Article

References (135)

1. A receptors by the GABA-agonist THIP (4,5,6,7-tetrahydroisoxazolo[5,4-c]pyridin-3-ol) in cultured rat cerebellar granule cells is prevented by inhibition of polyamine biosynthesis. J. Neurosci. Res. 39, 656-662.
2. Altman, J., 1972. Postnatal development of the cerebellar cortex in the rat: II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145, 399-464.
3. Altman, J., 1975. Postnatal development of the cerebellar cortex in the rat: IV. Spatial organization of bipolar cells, parallel fibers, and glial palisades. J. Comp. Neurol. 163, 427-464.
4. Balazs, R., Hack, N., Jørgensen, O.S., 1988. Stimulation of the N-methyl-D-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci. Lett. 87, 80-86.
5. Balazs, R., Hack, N., Jørgensen, O.S., 1990. Selective stimulations of excitatory amino acid receptor subtypes and the survival of cerebellar granule cells in culture: effect of kainic acid. Neuroscience 37, 251-258.
6. A receptor subunit mRNA expression in cultured cerebellar granule neurons. J. Neurosci. 13, 1784-1792.
7. A receptor subunit mRNAs in rat cerebellar granule neurons: importance of environmental cues. J. Neurochem. 66, 1347-1353.
8. Belhage, B., Hansen, G.H., Schousboe, A., Meier, E., 1988. GABA agonist promoted formation of low affinity GABA receptors on cerebellar granule cells is restricted to early development. Int. J. Dev. Neurosci. 6, 125-128.
9. 2/3-subunits. J. Biol. Chem. 266, 4478-4483.
10. A receptor subtypes containing the δ subunit in rat brain. FEBS Lett. 283, 145-149.
11. 1 benzodiazepine receptor subclass. J. Neurochem. 37, 333-341.
12. A receptors. J. Physiol. 497, 753-759.
13. Bureau, M., Olsen, R.W., 1990. Multiple distinct subunits of the γ-aminobutyric acid-A receptor protein show different ligand-binding affinities. Mol. Pharmacol. 37, 497-502.
14. A receptor subtypes: ligand binding heterogeneity demonstrated by photoaffinity labeling and autoradiography. J. Neurochem. 61, 1479-1491.
15. Candy, J.M., Martin, I.L., 1979. The postnatal development of the benzodiazepine receptor in the cerebral cortex and cerebellum of the rat. J. Neurochem. 32, 655-658.
16. A receptors. J. Neurosci. Res. 50, 1053-1062.
17. A receptor. J. Neurosci. 16, 5415-5424.
18. Chisholm, J., Kellogg, C., Lippa, A., 1983. Development of benzodiazepine binding subtypes in three regions of rat brain. Brain Res. 267, 388-391.
19. Connolly, C.N., Krishek, B.J., McDonald, B.J., Smart, T.G., Moss, S.J., 1996. Assembly and cell surface expression of heteromeric and homomeric γ-aminobutyric acid A receptors. J. Biol. Chem. 271, 89-96.
20. Coyle, J.T., Enna, S.J., 1976. Neurochemical aspects of the ontogenesis of GABAergic neurons in the rat brain. Brain Res. 111, 119-133.
21. 1 cDNA: a GABA receptor subunit highly expressed in the retina. Proc. Natl. Acad. Sci. USA 88, 2673-2677.
22. +- and kainate-mediated depolarization on survival and functional maturation of GABAergic and glutamatergic neurons in cultures of dissociated mouse cerebellum. Neurochem. Res. 21, 267-275.
23. A receptor subunit. Nature 385, 820-823.
24. - channel complex. J. Neurosci. 8, 602-614.
25. Drejer, J., Schousboe, A., 1989. Selection of a pure cerebellar granule cell culture by kainate treatment. Neurochem. Res. 14, 751-754.
26. Ebert, B., Thompson, S.A., Saounatsou, K., McKernan, R., Krogsgaard-Larsen, P., Wafford, K.A., 1997. Differences in agonist/antagonist binding affinity and receptor transduction using recombinant human γ-aminobutyric acid type A receptors. Mol. Pharmacol. 52, 1150-1156.
27. Eccles, J.C., 1970. Neurogenesis and morphogenesis in the cerebellar cortex. Proc. Natl. Acad. Sci. USA 66, 294-301.
28. Eins, E., Spoerri, P.E., Heyder, E., 1983. GABA or sodium bromide-induced plasticity of neuntes of mouse neuroblastoma cells in cultures. A quantitative study. Cell Tissue Res. 229, 457-460.
29. A receptor subunits in soma and processes of cerebellar granule cells: effects of maturation and a GABA agonist. Int. J. Dev. Neurosci. 13, 417-428.
30. Fagg, G.E., Foster, A.C., 1983. Amino acid neurotransmitters and their pathways in the mammalian central nervous system. Neuroscience 9, 701-719.
31. 3H-THIP to rat brain synaptic membranes. J. Neurochem. 38, 1123-1129.
32. Gallo, V., Kingsbury, A., Balazs, R., Jørgensen, O.S., 1987. The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7, 2203-2213.
33. 1 subunit mRNA in the rat brain. J. Neurobiol. 21, 1169-1179.
34. A receptor δ subunit is selectively modulated by depolarization in cultured rat cerebellar granule neurons. J. Neurosci. 17, 2391-2399.
35. 2 subunit gene of γ-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. USA 92, 7749-7753.
36. A receptor in the rat brain. J. Neurosci. 14, 7168-7179.
37. A receptor in the rat nervous system. J. Comp. Neurol. 365, 504-510.
38. A receptors. Mol. Pharmacol. 43, 970-975.
39. Hadingham, K.L., Wingrove, P.B., Wafford, K.A., Bain, C., Kemp, J.A., Palmer, K.J., Wilson, A.W., Wilcox, A.S., Sikela, J.M., Regan, C.I., Whiting, P.J., 1993b. Role of the β subunit in determining the pharmacology of human γ-aminobutyric acid type a receptor. Mol. Pharmacol. 44, 1211-1218.
40. Hansen, G.H., Meier, E., Schousboe, A., 1984. GABA influences the ultrastructure composition of cerebellar granule cells during development in culture. Int. J. Dev. Neurosci. 2, 247-257.
41. Hansen, G.H., Meier, E., Abraham, J., Schousboe, A., 1987. Trophic effects of GABA on cerebellar granule cells in culture. In: Redburn, D.A., Schousboe, A. (Eds.), Neurotrophic Activity of GABA during Development. Alan R. Liss, New York, pp. 109-138.
42. A-receptors in the plasma membrane of cultured cerebellar granule cells: an immunocytochemical study. Neurosci. Lett. 124, 162-165.
43. A receptor subunits. Mol. Brain Res. 28, 338-342.
44. Hertz, L., Juurlink, B.H.J., Szuchet, S., 1985. Cell cultures. In: Lajtha, A. (Ed.), Handbook of Neurochemistry, Vol. 8. Plenum, New York, pp. 603-661.
45. A receptors in rat cerebellum and thalamus. Eur. J. Pharmacol. 310, 225-233.
46. 6 subunits. J. Neurosci. 18, 2449-2457.
47. 6 subunit gene inactivation inhibits δ subunit expression. J. Neurosci. 17, 1350-1362.
48. A /benzodiazepine receptor. J. Neurochem. 60, 961-971.
49. A /benzodiazepine receptor from rat cerebellum. J. Neurochem. 63, 371-374.
50. A receptor maintaining their individual benzodiazepine-binding specificities. J. Neurochem. 66, 685-691.
51. A receptor subtypes in developing hippocampal neurons. Neuron 7, 927-936.
52. A receptor mRNAs and increases ligand binding. J. Neurochem. 61, 2334-2337.
53. Komuro, H., Rakic, P., 1998. Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J. Neurosci. 18, 1478-1490.
54. 3H]Ro 15-4513 binding sites. Neuroscience 53, 483-488.
55. Korpi, E.R., Kuner, T., Seeburg, P.H., Lüddens, H., 1995. Selective antagonist for the cerebellar granule cell-specific γ-aminobutyric acid type A receptor. Mol. Pharmacol. 47, 283-289.
56. Larsson, O.M., Drejer, J., Kvamme, E., Svenneby, G., Hertz, L., Schousboe, A., 1985. Ontogenetic development of glutamate and GABA metabolizing enzymes in cultured cerebral cortex interneurons and in cerebral cortex in vivo. Int. J. Dev. Neurosci. 3, 177-185.
57. Lasher, R.S., Zagon, I.S., 1972. The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res. 41, 482-488.
58. A receptor subunit mRNAs in the rat brain: II. Olfactory bulb and cerebellum. J. Neurosci. 12, 1063-1076.
59. A receptor subunit mRNAs in the rat brain: III. Embryonic and postnatal development. J. Neurosci. 12, 4151-4172.
60. A receptor selective for a behavioral alcohol antagonist. Nature 346, 648-651.
61. A /benzodiazepine receptor complex. J. Recept. Res. 11, 535-551.
62. A receptor channels. Annu. Rev. Neurosci. 17, 569-602.
63. Madtes, P.C., Redburn, D.A., 1983a. GABA as a trophic factor during development. Life Sci. 33, 979-984.
64. Madtes, P.C., Redburn, D.A., 1983b. Synaptic interactions in the GABA system during postnatal development in retina. Brain Res. Bull. 101, 741-745.
65. 3H]Ro 15-4513 binding to intact cultured cerebellar granule cells. Eur. J. Pharmacol. 169, 53-60.
66. A receptor structure and physiological properties in cultured cerebellar granule neurons. Neuron 13, 149-158.
67. Meier, E., Schousboe, A., 1982. Differences between GABA receptor binding to membranes from cerebellum during postnatal development and from cultured cerebellar granule cells. Dev. Neurosci. 5, 546-553.
68. Meier, E., Drejer, J., Schousboe, A., 1983. Trophic actions of GABA on the development of physiologically active GABA receptors. In: Mandel, P., DeFeudis, F.V. (Eds.), CNS-Receptors from Molecular Pharmacology to Behavior. Raven Press, New York, pp. 47-58.
69. Meier, E., Drejer, J., Schousboe, A., 1984. GABA induces functionally active low-affinity GABA receptors on cultured cerebellar granule cells. J. Neurochem. 43, 1737-1744.
70. Meier, E., Hansen, G.H., Schousboe, A., 1985. The trophic effect of GABA on cerebellar granule cells is mediated by GABA-receptors. Int. J. Dev. Neurosci. 3, 401-407.
71. Meier, E., Belhage, B., Drejer, J., Schousboe, A., 1987. The expression of GABA receptors on cultured cerebellar granule cells is influenced by GABA. In: Redburn, D.A., Schousboe, A. (Eds.), Neurotrophic Activity of GABA During Development. Alan R. Liss, New York, pp. 139-159.
72. Meier, E., Jørgensen, O.S., Schousboe, A., 1987b. Effect of repeated THIP treatment on postnatal neural development in rats. J. Neurochem. 49, 1462-1470.
73. Messer, A., 1977. The maintenance and identification of mouse cerebellar granule cells in monolayer cultures. Brain Res. 130, 1-12.
74. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15, 2948-2960.
75. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J. Neurosci. 16, 103-114.
76. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693-1703.
77. 3 cDNA. Biochim. Biophys. Acta 1305, 15-18.
78. Olsen, R.W., Bergman, M.O., Van Ness, P.C., Lummis, S.C., Watkins, A.E., Napias, C., Greenlee, D.V., 1981. γ-Aminobutyric acid receptor binding in mammalian brain. Heterogeneity of binding sites. Mol. Pharmacol. 19, 217-227.
79. A receptor subtypes: autoradiographic comparison of GABA, benzodiazepine, and convulsant binding sites in the rat central nervous system. J. Chem. Neuroanat. 3, 59-76.
80. Palacios, J.M., Kuhar, M.J., 1982. Ontogeny of high-affinity GABA and benzodiazepine receptors in the rat cerebellum: an autoradiographic study. Dev. Brain Res. 2, 531-539.
81. 3H]GABA from neuron-and glia-enriched cultures of cells dissociated from rat cerebellum. Brain Res. 206, 485-489.
82. Peng, L., Juurlink, B.H.J., Hertz, L., 1991. Difference in transmitter release, morphology, and ischemia-induced cell injury between cerebellar granule cell cultures developing in the presence of and in the absence of a depolarizing potassium concentration. Dev. Brain Res. 63, 1-12.
83. A receptor subpopulations. J. Biol. Chem. 268, 3753-3757.
84. A receptors of adult rat cerebellum demonstrates two a subunits per receptor oligomer. J. Biol. Chem. 270, 21285-21290.
85. A receptor stimulation. J. Neurochem. 68, 631-639.
86. 5-subunit creates novel type II benzodiazepine receptor pharmacology. J. Neurochem. 54, 1802-1804.
87. A-benzodiazepine receptors produced in transfected cells. Science 245, 1389-1392.
88. A receptor subunit for benzodiazepine pharmacology. Nature 338, 582-585.
89. Quirk, K., Gillard, N.P., Ragan, C.I., Whiting, P.J., McKernan, R.M., 1994. Model of subunit composition of γ-aminobutyric acid A receptor subtypes expressed in rat cerebellum with respect to their a and γ/δsubunits. J. Biol. Chem. 269, 16020-16028.
90. Rakic, P., 1973. Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar, stellate and basket neurons. J. Comp. Neurol. 147, 523-540.
91. Rakic, P., Sidman, R.L., 1973. Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J. Comp. Neurol. 152, 103-132.
92. Richards, J.G., Möhler, H., Haefely, W., 1986. Mapping benzodiazepine receptors in the CNS by radiohistochemistry and immunohistochemistry. In: Panula, P., Pairannta, H., Soinita, S. (Eds.), Neurohistochemistry: Modern Methods and Applications. Alan R. Liss, New York, pp. 629-677.
93. A /benzodiazepine receptors: cellular and subcellular localization in the CNS with monoclonal antibodies. J. Neurosci. 7, 1866-1886.
94. A receptor subunit mRNAs in individual cerebellar neurons after whole-cell recordings. J. Neurochem. 63, 2357-2360.
95. A receptor subunits: role of the δ subunit. J. Neurosci. 14, 7077-7086.
96. A receptor isoforms. Mol. Pharmacol. 49, 567-579.
97. A receptor shows a ligand-gated receptor super-family. Nature 328, 221-227.
98. 3H-taurine from cultured GABAergic and glutamatergic neurons. J. Neurochem. 53, 1309-1315.
99. Schousboe, A., Meier, E., Drejer, J., Hertz, L., 1989. Preparation of primary cultures of mouse (rat) cerebellar granule cells. In: Shahar, A., De Vellis, J., Vernadakis, A., Haber, B. (Eds.), A Dissection and Tissue Culture Manual of the Nervous System. Alan R. Liss, New York, pp. 203-206.
100. A receptor subunits exist in distinct neuronal subpopulations. Neuron 3, 327-337.
101. Sieghart, W., 1986. Comparison of benzodiazepine receptors in cerebellum and inferior colliculus. J. Neurochem. 47, 920-923.
102. 3H]Ro 15-4513: a biochemical and autoradiographic study. J. Neurochem. 48, 46-52.
103. A receptors. TiPS 16, 162-168.
104. A receptors in the cerebellum of rat, cat and monkey using monoclonal antibodies. J. Neurosci. 9, 2197-2209.
105. Spoerri, P.E., Wolff, J.R., 1981. Effect of GABA-administration on murine neuroblastoma cells in culture. Cell Tiss. Res. 218, 567-579.
106. Squires, R.F., Benson, D.I., Braestrup, C., Coupet, J., Klepner, C.A., Myers, V., Beer, B., 1979. Some properties of brain specific benzodiazepine receptor: New evidence for multiple receptors. Pharmacol. Biochem. Behav. 10, 825-830.
107. Squires, R.F., Saederup, E., Damgaard, I., Schousboe, A., 1990. Development of benzodiazepine and picrotoxin (t-butylbicyclo-phosphorothionate) binding sites in rat cerebellar granule cells in culture. J. Neurochem. 54, 473-478.
108. A receptors. Biochem. J. 310, 1-9.
109. A receptor subtypes expressed in cerebellar granule cells: a developmental study. J. Neurochem. 62, 2037-2044.
110. 6 subunit-like immunoreactivity in rat brain. Neurosci. Lett. 144, 53-56.
111. 6 subunit expression by a cyclic AMP-mediated signalling mechanism in cerebellar granule cells in primary culture. J. Neurochem. 67, 434-437.
112. 6 subunits in cultured rat cerebellar granule cells. Neuropharmacology 35, 1337-1346.
113. A receptors. Neuropharmacology 35, 1375-1382.
114. 6 subunit. J. Neurosci. 16, 3630-3640.
115. A receptor subtype. J. Neurosci. 17, 2728-2737.
116. A receptor subtype that is insensitive to diazepam. J. Pharmacol. Exp. Ther. 257, 1236-1242.
117. A receptor subtypes. Mol. Pharmacol. 43, 240-244.
118. Wafford, K.A., Bain, C.J., Whiting, P.J., Kemp, J.A., 1993b. A functional comparison of the role of y subunits in recombinant γ-aminobutyric acid type A/benzodiazepine receptors. Mol. Pharmacol. 43, 437-442.
119. A receptor beta subunit. Neuron 12, 775-782.
120. A receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur. J. Neurosci. 9, 533-548.
121. 3H-muscimol binding to mouse brain membranes. Biochem. Pharmacol. 28, 1123-1128.
122. A receptors is essential for benzodiazepine agonist binding. J. Biol. Chem. 267, 1426-1429.
123. 4 subunit. FEBS Lett. 289, 227-230.
124. A receptor diversity. Neuropharmacology 35, 1139-1160.
125. Wolff, J.R., Foo, F., Dames, W., 1979. Plasticity in dendrites shown by continuous GABA administration in superior cervical ganglion of adult rat. Nature 274, 72-74.
126. Wolff, J.R., Joo, F., Kasa, P., 1987. Synaptic, metabolic and morphogenetic effects of GABA in the superior cervical ganglion of rats. In: Redburn, D.A., Schousboe, A. (Eds.), Neurotrophic Activity of GABA during Development. Alan R. Liss, New York, pp. 221-252.
127. Young, A.B., Oster-Granite, M.C., Herndon, R.M., Snyder, S.H., 1974. Glutamic acid: selective depletion by viral induced granule cell loss in hamster cerebellum. Brain Res. 73, 1-13.
128. Young, S.W. III, Niehoff, D., Kuhar, M.J., Beer, B., Lippa, A.S., 1981. Multiple benzodiazepine receptor localization by light microscopic radiohistochemistry. J. Pharmacol. Exp. Ther. 216, 425-430.
129. 3H]flunitrazepam binding sites during postnatal development of the mouse cerebellum. Dev. Brain Res. 61, 63-71.
130. A receptor subunit mRNA occurs only after cerebellar granule cell migration. Dev. Brain Res. 75, 91-103.
131. Zheng, T.M., Zhu, W.J., Puia, G., Vicini, S., Grayson, D.R., Costa, E., Caruncho, H.J., 1994. Changes in γ-aminobutyrate type A receptor subunit mRNAs, translation product expression, and receptor function during neuronal maturation in vitro. Proc. Natl. Acad. Sci. USA 91, 10952-10956.
132. A channel deactivation by altering kinetics of desensitized states. J. Neurosci. 17, 4022-4031.
133. Zhu, W.J., Vicini, S., Harris, B.T., Grayson, D.R., 1995. NMDA-mediated modulation of γ-aminobutyric acid type A receptor function in cerebellar granule neurons. J. Neurosci. 15, 7692-7701.
134. A receptors. J. Neurosci. 16, 6648-6656.
135. A receptor in the rat brain. Neurosci. Lett. 127, 125-128.