Steroid modulation of GABAA receptors:from molecular mechanisms to CNS roles in reproduction, dysfunction and drug abuse

Advances in Molecular and Cell Biology

Volumn 32, Issue , 2004, Pages 219-250

  Henderson, Leslie P ^a   Jorge, Juan Carlos ^a  

^a UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 11844274899     PISSN: 15692558     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1569-2558(03)32010-7     Document Type: Review

References (246)

1. H. Betz Ligand-gated ion channels in the brain: the amino acid receptor superfamily Neuron 5 1990 383 392
2. R.T. Boyd The molecular biology of neuronal nicotinic acetylcholine receptors Crit. Rev. Toxicol. 27 3 1997 299 318
3. H. Betz J. Kuhse V. Schmieden B. Laube J. Kirsch R.J. Harvey Structure and functions of inhibitory and excitatory glycine receptors Ann. NY Acad. Sci. 868 1999 667 676
4. M.B. Jackson J.L. Yakel The 5-HT3 receptor channel Annu. Rev. Physiol. 57 1995 447 468
5. A receptors: classification on the basis of subunit structure and receptor function Pharmacol. Rev. 50 2 1998 291 313
6. A receptors Trends Pharmacol. Sci. 16 5 1995 162 168
7. A receptor shows a ligand-gated receptor super-family Nature 328 1987 221 227
8. A receptors Brain Res. Revs. 29 2–3 1999 196 217
9. P.J. Whiting The GABA-A receptor gene family: new targets for therapeutic intervention Neurochem. Int. 34 5 1999 387 390
10. P. Whiting T.P. Bonnert R.M. McKernan S. Farrar B. Le Bourdellés R.P. Heavens D.W. Smith L. Hewson M.R. Rigby D.J.S. Sirinathsinghji S.A. Thompson K.A. Wafford Molecular and functional diversity of the expanding GABA-A receptor gene family Ann. NY Acad. Sci. 868 1999 645 653
11. A receptor channels Annu. Rev. Neurosci. 17 1994 569 602
12. A receptor heterogeneity is increased by alternative splicing of a novel β-subunit gene transcript J. Neurochem. 56 4 1991 1437 1440
13. A receptor FEBS Lett. 331 3 1993 211 216
14. 2 subunit, one of which contains a protein kinase C phosphorylation site Proc. Natl Acad. Sci. USA 87 1990 9966 9970
15. 2-subunit in mice by alternative splicing J. Neurochem. 56 2 1991 713 715
16. A receptor J. Biol. Chem. 267 1992 14470 14476
17. 2 subunit J. Neurochem. 62 1 1994 10 16
18. A receptor Mol. Brain Res. 28 1995 175 179
19. 3 subunit (GABRB3) J. Biol. Chem. 268 6 1993 4420 4428
20. A receptor function J. Neurochem. 63 3 1994 1167 1170
21. C receptors: relatively simple transmitter-gated ion channels? Trends Pharmacol. Sci. 17 9 1996 319 323
22. A receptor subunit in tissues of the reproductive system J. Biol. Chem. 272 24 1997 15346 15350
23. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits J. Comp. Neurol. 359 1 1995 154 194
24. A/benzodiazepine receptors J. Neurochem. 63 4 1994 1466 1476
25. 1 does not exist in combination with another γ-subunit Mol. Pharmacol. 45 1994 1061 1070
26. A receptors from rat brain Eur. J. Pharmacol. 290 3 1995 175 181
27. A receptor channel function in the nervous system Prog. Neurobiol. 42 4 1994 489 537
28. E. Cherubini J.L. Gaiarsa Y. Ben-Ari GABA: an excitatory transmitter in early postnatal life Trends Neurosci. 14 12 1991 515 519
29. B. Sakmann J. Bormann O.P. Hamill Ion transport by single receptor channels Cold Spring Harb. Symp. Quant. Biol. 48 1 1983 247 257
30. J. Bormann O.P. Hamill B. Sakmann Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones J. Physiol. (Lond.) 385 1987 243 286
31. J. Bormann D.E. Clapham γ-Aminobutyric acid receptor channels in adrenal chromaffin cells: a patch-clamp study Proc. Natl Acad. Sci. USA 82 7 1985 2168 2172
32. − channels in cultured astrocytes Proc. Natl Acad. Sci. USA 85 23 1988 9336 9340
33. A receptor main conductance state of mouse spinal cord neurones in culture J. Physiol. (Lond.) 410 1989 479 499
34. − channels determined from stability plots, dwell-time distributions, and adjacent-interval durations J. Neurosci. 9 4 1989 1314 1324
35. A receptors Neuron 4 5 1990 759 765
36. C.F. Newland D. Colquhoun S.G. Cull-Candy Single channels activated by high concentrations of GABA in superior cervical ganglion neurones of the rat J. Physiol. (Lond.) 432 1991 203 233
37. R. Schneggenburger A. Konnerth GABA-mediated synaptic transmission in neuroendocrine cells: a patch-clamp study in pituitary slice preparation Pflügers Arch. 421 4 1992 364 373
38. A receptor complex in cultured rat neurones J. Physiol. (Lond.) 447 1992 587 625
39. A receptor single-channel kinetic properties of mouse spinal cord neurons in culture J. Physiol. (Lond.) 456 1992 215 245
40. 2S subunits produce unique ion channels with dissimilar single-channel properties J. Neurosci. 13 4 1993 1429 1440
41. A receptors open? Neuron 12 1 1994 61 71
42. A receptor channels of mouse spinal cord neurones in culture J. Physiol. (Lond.) 475.1 1994 69 82
43. A receptor of rat posterior pituitary nerve terminals J. Neurophysiol. 73 3 1995 1135 1144
44. A receptors suggest differential targeting of receptor subtypes J. Neurosci. 19 8 1999 2960 2973
45. A receptors from mice lacking the γ2 subunit J. Physiol. (Lond.) 527.1 2000 11 31
46. A. Konnerth I. Llano C.M. Armstrong Synaptic currents in cerebellar Purkinje cells Proc. Natl Acad. Sci. USA 87 7 1990 2662 2665
47. P. Vincent C.M. Armstrong A. Marty Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization J. Physiol. (Lond.) 456 1992 453 471
48. A receptors Neuropharmacology 35 9/10 1996 1375 1382
49. A receptors in cultured murine cerebellar granule cells J. Physiol. (Lond.) 503.2 1997 353 369
50. A receptors and glomerular geometry Neuron 20 1998 783 795
51. G.L. Collingridge P.W. Gage B. Robertson Inhibitory post-synaptic currents in rat hippocampal CA1 neurones J. Physiol. (Lond.) 356 1984 551 564
52. F.A. Edwards A. Konnerth B. Sakmann Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study J. Physiol. (Lond.) 430 1990 213 249
53. A,slow J. Neurosci. 18 4 1998 1305 1317
54. A IPSCs during development in rat hippocampal or cerebellar slices J. Physiol. (Lond.) 521.2 1999 437 449
55. A receptors J. Neurosci. 19 7 1999 2474 2488
56. B autoreceptors J. Physiol. (Lond.) 502.1 1997 91 104
57. A receptor-mediated responses in the ventromedial nucleus of the hypothalamus of female and male neonatal rats Neuroendocrinology 64 2 1996 103 113
58. D. Haage S. Johansson Neurosteroid modulation of synaptic and GABA-evoked currents in neurons from the rat medial preoptic nucleus J. Neurophysiol. 82 1 1999 143 151
59. A receptors in neurons expressing γ1 subunit mRNA in the preoptic area of the rat J. Neurophysiol. 81 1 1999 192 203
60. A receptor-mediated currents in the rat forebrain J. Neurophysiol. 83 2000 3299 3309
61. A receptors underlying inhibitory synaptic currents in neocortical pyramidal neurons J. Neurosci. 17 19 1997 7220 7227
62. A receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord J. Neurosci. 19 17 1999 7342 7355
63. R. Schneggenburger J. López-Barneo A. Konnerth Excitatory and inhibitory synaptic currents and receptors in rat medial septal neurones J. Physiol. (Lond.) 445 1992 261 276
64. A channel responses to brief agonist pulses Neuron 15 1 1995 181 191
65. M.V. Jones G.L. Westbrook The impact of receptor desensitization on fast synaptic transmission Trends Neurosci. 19 3 1996 96 101
66. A channel deactivation by altering kinetics of desensitized states J. Neurosci. 17 11 1997 4022 4031
67. A receptor J. Neurosci. 18 21 1998 8590 8604
68. A receptor subtypes Pharmacol. Rev. 47 2 1995 181 234
69. A receptor function Trends Pharmacol. Sci. 16 9 1995 295 303
70. T. Narahashi K.S. Ginsburg K. Nagata J.H. Song H. Tatebayashi Ion channels as targets for insecticides Neurotoxicology 19 4–5 1998 581 590
71. C.F. Zorumski J. Yang Non-competitive inhibition of GABA currents by phenothiazines in cultured chick spinal cord and rat hippocampal neurons Neurosci. Lett. 92 1 1988 86 91
72. A receptor Neurosci. Lett. 189 1 1995 35 38
73. 35S]TBPS binding J. Pharmacol. Exp. Ther. 279 1 1996 186 193
74. A receptors Neuropharmacology 43 4 2002 619 633
75. A channel heterogeneity Mol. Neurobiol. 19 2 1999 97 110
76. A, and nicotinic acetylcholine receptors provide new insights into the ligand-gated ion channel receptor superfamily Int. Rev. Neurobiol. 42 1998 285 332
77. A. Revelli J. Tesarik M. Massobrio Nongenomic effects of neurosteroids Gynecol. Endocrinol. 12 1 1998 61 67
78. E.E. Baulieu Neurosteroids: a novel function of the brain Psychoneuroendocrinology; 23 8 1998 963 987
79. N.A. Compagnone S.H. Mellon Neurosteroids: biosynthesis and function of these novel neuromodulators Front Neuroendocrinol. 21 1 2000 1 56
80. A receptor: mechanisms of action and physiological significance Prog. Neurobiol. 38 4 1992 379 395
81. R. Rupprecht C.A. Hauser T. Trapp F. Holsboer Neurosteroids: molecular mechanisms of action and psychopharmacological significance J. Steroid Biochem. Mol. Biol. 56 1–6 1996 163 168
82. M.A. Wilson GABA physiology: modulation by benzodiazepines and hormones Crit. Rev. Neurobiol. 10 1 1996 1 37
83. M. Bixo A. Andersson B. Winblad R.H. Purdy T. Bäckström Progesterone, 5α-pregnane-3,20-dione and 3α-hydroxy-5α-pregnane-20-one in specific regions of the human female brain in different endocrine states Brain Res. 764 1–2 1997 173 178
84. I. Sundström T. Bäckström M. Wang T. Olsson L. Seippel M. Bixo Premenstrual syndrome, neuroactive steroids and the brain Gynecol. Endocrinol. 13 3 1999 206 220
85. C. Lacroix J. Fiet J.P. Benais B. Gueux R. Bonete J.M. Villette B. Gourmel C. Dreux Simultaneous radioimmunoassay of progesterone, androst-4-enedione, pregnenolone, dehydroepiandrosterone and 17-hydroxyprogesterone in specific regions of human brain J. Steroid Biochem. 28 3 1987 317 325
86. A. Lanthier V.V. Patwardhan Sex steroids and 5-en-3 beta-hydroxysteroids in specific regions of the human brain and cranial nerves J. Steroid Biochem. 25 3 1986 445 449
87. D.M. Herrington DHEA: a biological conundrum J. Lab. Clin. Med. 131 4 1998 292 294
88. M.E. Blasberg S. Robinson L.P. Henderson A.S. Clark Inhibition of estrogen-induced sexual receptivity by androgens: role of the androgen receptor Horm. Behav. 34 3 1998 283 293
89. A receptor activity by alphaxalone Br. J. Pharmacol. 90 3 1987 491 500
90. A receptor by progesterone metabolites Proc. R Soc. Lond. B 231 1987 359 369
91. A receptor by depressant barbiturates and pregnane steroids Br. J. Pharmacol. 94 4 1988 1257 1269
92. A receptor α subunit Mol. Pharmacol. 44 1 1993 87 92
93. A receptor complex J. Pharmacol. Exp. Ther. 241 1 1987 346 353
94. K.W. Gee M.B. Bolger R.E. Brinton H. Coirini B.S. McEwen Steroid modulation of the chloride ionophore in rat brain: structure–activity requirements, regional dependence and mechanism of action J. Pharmacol. Exp. Ther. 246 2 1988 803 812
95. A receptor pharmacology of enantiomers of dehydroepiandrosterone sulfate, pregnenolone sulfate, and (3α,5β)-3hydroxypregnan-20-one sulfate J. Med. Chem. 41 14 1998 2604 2613
96. A receptor modulation and anesthesia J. Pharmacol. Exp. Ther. 293 3 2000 1009 1016
97. K.W. Gee Steroid modulation of the GABA/benzodiazepine receptor-linked chloride ionophore Mol. Neurobiol. 2 1988 291 317
98. D.M. Turner R.W. Ransom J.S.J. Yang R.W. Olsen Steroid anesthetics and naturally occurring analogs modulate the γ-aminobutyric acid receptor complex at a site distinct from barbiturates J. Pharmacol. Exp. Ther. 248 1989 960 966
99. A.L. Morrow J.R. Pace R.H. Purdy S.M. Paul Characterization of steroid interactions with γ-aminobutyric acid receptor-gated chloride ion channels: evidence for multiple steroid recognition sites Mol. Pharmacol. 37 2 1990 263 270
100. A receptor isoforms Can. J. Physiol. (Lond.) Pharmacol. 76 9 1998 909 920
101. A receptor function through distinct sites Brain Res. 830 1 1999 72 87
102. C.F. Zorumski S.J. Mennerick D.F. Covey Enantioselective modulation of GABAergic synaptic transmission by steroids and benz[ e ]indenes in hippocampal microcultures Synapse 29 2 1998 162 171
103. A receptor Science 232 1986 1004 1007
104. N.L. Harrison S. Vicini J.L. Barker A steroid anesthetic prolongs inhibitory postsynaptic currents in cultured rat hippocampal neurons J. Neurosci. 7 1987 604 609
105. A. Chvátal H. Kettenmann Effect of steroids on γ-aminobutyrate-induced currents in cultured rat astrocytes Plügers Arch. 419 3–4 1991 263 266
106. A.B. Brussaard J. Wossink J.C. Lodder K.S. Kits Progesterone-metabolite prevents protein kinase C-dependent modulation of γ-aminobutyric acid type A receptors in oxytocin neurons Proc. Natl Acad. Sci. USA 97 7 2000 3625 3630
107. A. Fáncsik D.M. Linn J.G. Tasker Neurosteroid modulation of GABA IPSCs is phosphorylation dependent J. Neurosci. 20 9 2000 3067 3075
108. A receptor of mouse spinal neurones in culture Exp. Physiol. 75 2 1990 199 209
109. A receptor-mediated IPSCs by neuroactive steroids in a rat hypothalamo-hypophyseal coculture model J. Physiol. (Lond.) 500 2 1997 475 485
110. K. Tsutsui K. Ukena Neurosteroids in the cerebellar Purkinje neuron and their actions (Review) Int. J. Mol. Med. 4 1 1999 49 56
111. J.L. Barker N.L. Harrison G.D. Lange D.G. Owen Potentiation of γ-aminobutyric-acid-activated chloride conductance by a steroid anaesthetic in cultured rat spinal neurones J. Physiol. (Lond.) 386 1987 485 501
112. S.J. Moss T.G. Smart Modulation of amino acid-gated ion channels by protein phosphorylation Int. Rev. Neurobiol. 39 1996 1 52
113. S. Kellenberger P. Malherbe E. Sigel Function of α1β2γ2S γ-aminobutyric acid type A receptor is modulated by protein kinase C via multiple phosphorylation sites J. Biol. Chem. 267 36 1992 25660 25663
114. A receptor by cAMP-dependent protein kinase and by protein kinase C: analysis of the substrate domain Neurochem. Res. 18 1 1993 95 100
115. A receptor function by protein kinase C phosphorylation Neuron 12 5 1994 1081 1095
116. A receptor: role of desensitization Mol. Pharmacol. 41 6 1992 1116 1123
117. A receptors Mol. Brain Res. 52 1997 173 181
118. A receptor-mediated currents via a reduction of channel opening frequency Brain Res. 489 1 1989 190 194
119. A receptor complex reveals that it may act via the picrotoxin site J. Pharmacol. Exp. Ther. 282 2 1997 827 833
120. A receptor Neuroscience 45 1 1991 127 135
121. A receptor Brain Res. 526 1 1990 143 146
122. M.D. Majewska R.D. Schwartz Pregnenolone-sulfate: an endogenous antagonist of γ-aminobutyric acid receptor complex in brain? Brain Res. 404 1–2 1987 355 360
123. S.L. Hansen B. Fjalland M.B. Jackson Differential blockade of γ-aminobutyric acid type A receptors by the neuroactive steroid dehydroepiandrosterone sulfate in posterior and intermediate pituitary Mol. Pharmacol. 55 3 1999 489 496
124. A receptor-mediated chloride uptake Brain Res. 790 1–2 1998 334 338
125. A receptors in ventral midbrain neurons by a neurosteroid dehydroepiandrosterone sulfate Synapse 16 1994 113 122
126. M.D. Majewska J.M. Mienville S. Vicini Neurosteroid pregnenolone sulfate antagonizes electrophysiological responses to GABA in neurons Neurosci. Lett. 90 3 1988 279 284
127. A receptor desensitization J. Neurosci. 20 10 2000 3571 3579
128. N.C. Lan K.W. Gee M.B. Bolger J.S. Chen Differential responses of expressed recombinant human γ-aminobutyric acidA receptors to neurosteroids J. Neurochem. 57 5 1991 1818 1821
129. A receptor on the response to a neurosteroid Eur. J. Pharmacol. 206 1 1991 77 80
130. A receptor subunit composition? Receptors Channels 1 2 1993 135 142
131. A receptors by pregnanediols Neuropharmacology 35 9/10 1996 1223 1231
132. K.L. Hadingham E.M. Garrett K.A. Wafford C. Bain R.P. Heavens D.J. Sirinathsinghji P.J. Whiting Cloning of cDNAs encoding the human γ-aminobutyric acid type A receptor α6 subunit and characterization of the pharmacology of α6-containing receptors Mol. Pharmacol. 49 2 1996 253 259
133. A receptors Biochem. Biophys. Res. Commun. 219 2 1996 531 536
134. A receptors J. Neurosci. 16 21 1996 6648 6656
135. A receptors in cultured hippocampal neurons and transfected HEK-293 cells Neuropharmacology 35 9/10 1996 1161 1168
136. A receptor function by neuroactive steroids Brain Res. 819 1–2 1999 75 82
137. A receptors Int. Rev. Neurobiol. 46 2001 177 205
138. A receptors containing the delta subunit J. Neurosci. 22 5 2002 1541 1549
139. A receptors containing the δ subunit Neuropharmacology 43 4 2002 492 502
140. A receptors Neuropharmacology 43 4 2002 651 661
141. K.L. Hadingham P.R. Wingrove K.A. Wafford C. Bain J.A. Kemp K.J. Palmer A.W. Wilson A.S. Wilcox J.M. Sikela C.I. Ragan P.J. Whiting Role of the β subunit in determining the pharmacology of human γ-aminobutyric acid type A receptors Mol. Pharmacol. 44 6 1993 1211 1218
142. A and glycine receptors Neurochem. Int. 34 5 1999 447 452
143. S.L. Swope S.I. Moss L.A. Raymond R.L. Huganir Regulation of ligand-gated ion channels by protein phosphorylation Adv. Second Messenger Phosphoprotein Res. 33 1999 49 78
144. − currents Mol. Pharmacol. 39 6 1991 691 696
145. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon J. Neurosci. 12 3 1992 1040 1062
146. A receptor subunit conferring atypical functional properties J. Neurosci. 17 13 1997 5027 5037
147. A receptor ε and θ subunits display unusual structural variation between species and are enriched in the rat locus ceruleus J. Neurosci. 20 10 2000 3588 3595
148. N. Moragues P. Ciofi P. Lafon M.-F. Odessa G. Tramu M. Garret cDNA cloning and expression of a γ-aminobutyric acidA receptor ε-subunit in rat brain Eur. J. Neurosci. 12 2000 4318 4330
149. E. Boue-Grabot M. Roudbaraki G. Bascles G. Tramu B. Bloch M. Garret Expression of GABA receptor ρ subunits in rat brain J. Neurochem. 70 3 1998 899 907
150. K. Wegelius M. Pasternack J.O. Hiltunen C. Rivera K. Kaila M. Saarma M. Reeben Distribution of GABA receptor ρ subunit transcripts in the rat brain Eur. J. Neurosci. 10 1 1998 350 357
151. T.P. Bonnert R.M. McKernan S. Farrar B. le Bourdellés R.P. Heavens D.W. Smith L. Hewson M.R. Rigby D.J.S. Sirinathsinghji N. Brown K.A. Wafford P.J. Whiting θ, a novel γ-aminobutyric acid type A receptor subunit Proc. Natl Acad. Sci. USA 96 17 1999 9891 9896
152. 6 subunit gene inactivation inhibits δ subunit expression J. Neurosci. 17 4 1997 1350 1362
153. R. Makela M. Uusi-Oukari G.E. Homanics J.J. Quinlan L.L. Firestone W. Wisden E.R. Korpi Cerebellar γ-aminobutyric acid type A receptors: pharmacological subtypes revealed by mutant mouse lines Mol. Pharmacol. 52 3 1997 380 388
154. R.M. Mihalek P.K. Banerjee E.R. Korpi J.J. Quinlan L.L. Firestone Z.P. Mi C. Lagenaur V. Tretter W. Sieghart S.G. Anagnostaras J.R. Sage M.S. Fanselow A. Guidotti I. Spigelman Z. Li T.M. DeLorey R.W. Olsen G.E. Homanics Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor delta subunit knockout mice Proc. Natl Acad. Sci. USA 96 22 1999 12905 12910
155. A receptor δ subunit deletion prevents neurosteroid modulation of inhibitory synaptic currents in cerebellar neurons Neuropharmacology 43 4 2002 646 650
156. A receptors characterized by fluorescence resonance energy transfer-derived measurements of membrane potential J. Biol. Chem. 276 2001 38934 38939
157. A receptors Br. J. Pharmacol. 136 7 2002 965 974
158. A receptor subunit Nature 385 1997 820 823
159. A receptor subunit mRNAs in the mouse forebrain Neuropharmacology 43 4 2002 634 645
160. A receptor ε subunit results in insensitivity to anaesthetics Neuropharmacology 43 4 2002 662 668
161. A receptors change with hormonal state in the adult mouse J. Neurobiol. 50 2002 137 149
162. A/benzodiazepine receptors EMBO J. 9 10 1990 3261 3267
163. A receptor subunit expression in preoptic area and bed nucleus of the stria terminalis of female rat brain J. Neurosci. 15 3 1995 2328 2337
164. A receptor γ subunit mRNAs in sexually dimorphic regions of the rat brain Proc. R Soc. Lond. B 265 1998 1853 1859
165. A.R. Genazzani M.A. Palumbo A.A. de Micheroux P.G. Artini M. Criscuolo G. Ficarra A.L. Guo A. Benelli A. Bertolini F. Petraglia Evidence for a role for the neurosteroid allopregnanolone in the modulation of reproductive function in female rats Eur. J. Endocrinol. 133 3 1995 375 380
166. C.D. Kochakian Anabolic-androgenic steroids: a historical perspective C.E. Yesalis Anabolic Steroids in Sports and Exercise 1993 Human Kinetics Publishers Champaign IL 3 33
167. S.E. Lukas CNS effects and abuse liability of anabolic-androgenic steroids Annu. Rev. Pharmacol. Toxicol. 36 1996 333 357
168. 3H] 17α-methyl-testosterone in human subjects J. Endocrinol. 37 1 1967 37 55
169. S.J. Winters Androgens: endocrine physiology and pharmacology NIDA Res. Monogr. 102 1990 113 130
170. W. Schänzer G. Opfermann M. Donike Metabolism of stanozolol: identification and synthesis of urinary metabolites J. Steroid Biochem. 36 1–2 1990 153 174
171. R.C. Kammerer Drug testing and anabolic steroids C.E. Yesalis Anabolic Steroids in Sports and Exercise 1993 Human Kinetics Publishers Champaign, IL 283 308
172. F.H. Bronson Effects of prolonged exposure to anabolic steroids on the behavior of male and female mice Pharmacol. Biochem. Behav. 53 2 1996 329 334
173. F.H. Bronson K.Q. Nguyen J. De La Rosa Effect of anabolic steroids on behavior and physiological characteristics of female mice Physiol. Behav. 59 1 1996 49 55
174. M.E. Blasberg C.J. Langan A.S. Clark The effects of 17α-methyltestosterone, methandrostenolone, and nandrolone decanoate on the rat estrous cycle Physiol. Behav. 61 2 1997 265 272
175. M.D. Johnson Anabolic steroid use in adolescent athletes Pediatr. Clin. N. Am. 37 5 1990 1111 1123
176. W.W. Franke B. Berendonk Hormonal doping and androgenization of athletes: a secret program of the German Democratic Republic government Clin. Chem. 43 7 1997 1262 1279
177. R.H. Melloni Jr D.F. Connor P.T. Hang R.J. Harrison C.F. Ferris Anabolic-androgenic steroid exposure during adolescence and aggressive behavior in golden hamsters Physiol. Behav. 61 3 1997 359 364
178. G. Ågren I. Thiblin P. Tirassa T. Lundeberg C. Stenfors Behavioural anxiolytic effects of low-dose anabolic androgenic steroid treatment in rats Physiol. Behav. 66 3 1999 503 509
179. C.E. Yesalis C.K. Barsukiewicz A.N. Kopstein M.S. Bahrke Trends in anabolic-androgenic steroid use among adolescents Arch. Pediatr. Adolesc. Med. 151 12 1997 1197 1206
180. L.M. Kow C.V. Mobbs D.W. Pfaff Roles of second-messenger systems and neuronal activity in the regulation of lordosis by neurotransmitters, neuropeptides, and estrogen: a review Neurosci. Biobehav. Rev. 18 2 1994 251 268
181. A.E. Herbison C. Chapman R.G. Dyer Role of medial preoptic GABA neurones in regulating luteinising hormone secretion in the ovariectomised rat Exp. Brain Res. 87 2 1991 345 352
182. C. Decavel A.N. Van den Pol GABA: a dominant neurotransmitter in the hypothalamus J. Comp. Neurol. 302 1990 1019 1037
183. A receptor subunit expression Neuron 19 1997 1103 1114
184. A.E. Herbison Estrogen regulation of GABA transmission in rat preoptic area Brain Res. Bull. 44 4 1997 321 326
185. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid Nature 392 1998 926 930
186. 4 subunit in association with increased anxiety J. Neurosci. 18 14 1998 5275 5284
187. Y. Delville Progesterone-facilitated sexual receptivity: a review of arguments supporting a nongenomic mechanism Neurosci. Biobehav. Rev. 15 1991 407 414
188. C.A. Frye L.E. Bayon N.K. Pursnani R.H. Purdy The neurosteroids, progesterone and 3α,5α-THP, enhance sexual motivation, receptivity, and proceptivity in female rats Brain Res. 808 1998 72 83
189. M.M. McCarthy F.A. Beach Award Functional significance of steroid modulation of GABAergic neurotransmission: analysis at the behavioral, cellular, and molecular levels Horm. Behav. 29 1995 131 140
190. A receptor activity J. Neuroendocrinol. 11 11 1999 829 837
191. C.A. Frye K.R. Van Keuren P.N. Rao M.S. Erskine Progesterone and 3α-androstanediol conjugated to bovine serum albumin affects estrous behavior when applied to the MBH and POA Behav. Neurosci. 110 3 1996 603 612
192. C.A. Frye J.E. Duncan M. Basham M.S. Erskine Behavioral effects of 3α-androstanediol II: Hypothalamic and preoptic area actions via a GABAergic mechanism Behav. Brain Res. 79 1996 119 130
193. C.A. Frye S.G. Gardiner Progestins can have a membrane-mediated action in rat midbrain for facilitation of sexual receptivity Horm. Behav. 30 4 1996 682 691
194. C.A. Frye J.M. Vongher Progesterone has rapid and membrane effects in the facilitation of female mouse sexual behavior Brain Res. 815 1999 259 269
195. M.S. Erskine Serum 5α-androstane-3α,17β-diol increases in response to paced coital stimulation in cycling female rats Biol. Reprod. 37 1987 1139 1148
196. G. Verhoeven W. Heyns P. De Moor Ammonium sulfate precipitation as a tool for the study of androgen receptor proteins in rat prostrate and mouse kidney Steroids 6 1975 149 167
197. C.E. Roselli L.E. Horton J.A. Resko Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area Biol. Reprod. 37 1987 628 633
198. M.S. Erskine Effect of 5α-dihydrotestosterone and flutamide on the facilitation of lordosis by LHRH and naloxone in estrogen-primed female rats Physiol. Behav. 45 1989 753 759
199. D.A. Poulain J.B. Wakerley Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin Neuroscience 7 1982 773 808
200. A.B. Brussaard K.S. Kits T.A. de Vlieger Postsynaptic mechanism of depression of GABAergic synapses by oxytocin in the supraoptic nucleus of immature rat J. Physiol. (Lond.) 497 1996 495 507
201. A.J. Summerlee Extracellular recordings from oxytocin neurones during the expulsive phase of birth in unanaesthesized rats J. Physiol. (Lond.) 321 1981 1 9
202. G. Leng C.H. Brown J.A. Russell Physiological pathways regulating the activity of magnocellular neurosecretory cells Prog. Neurobiol. 57 1999 625 655
203. A receptors in the actions of alcohol and in alcoholism: recent advances Alcohol Alcohol. 29 2 1994 115 129
204. A receptors Brain Res. 805 1998 88 94
205. A receptors in the acute and chronic effects of ethanol Psychopharmacology 139 1–2 1998 2 19
206. H.E. Criswell T.J. McCown Z. Ming R.A. Mueller G.R. Breese Interactive role for neurosteroids in ethanol enhancement of γ-aminobutyric acid-gated currents from dissociated substantia nigra reticulata neurons J. Pharmacol. Exp. Ther. 291 3 1999 1054 1059
207. P.H. Janak J.E. Redfern H.H. Samson The reinforcing effects of ethanol are altered by the endogenous neurosteroid, allopregnanolone Alcohol Clin. Exp. Res. 22 5 1998 1106 1112
208. P. Bienkowski W. Kotowski Discriminative stimulus properties of ethanol in the rat: effects of neurosteroids and picrotoxin Brain Res. 753 2 1997 348 352
209. M.J. VanDoren D.B. Matthews G.C. Janis A.C. Grobin L.L. Devaud A.L. Morrow Neuroactive steroid 3α-hydroxy-5α-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol J. Neurosci. 20 5 2000 1982 1989
210. L.L. Devaud R.H. Purdy A.L. Morrow 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
211. A receptors to neuroactive steroids in rats during ethanol withdrawal J. Pharmacol. Exp. Ther. 278 1996 510 517
212. A. Romeo E. Brancati A. De Lorenzo P. Fucci C. Furnari E. Pompili G.F. Sasso G. Spalleta A. Troisi A. Pasini Marked decrease of plasma neuroactive steroids during alcohol withdrawal Clin. Neuropharmacol. 19 4 1996 366 369
213. H.J. Sturenburg U. Fries K. Kunze Glucocorticoids and anabolic/androgenic steroids inhibit the synthesis of GABAergic steroids in rat cortex Neuropsychobiology 35 3 1997 143 146
214. R.J. Baldessarini Drugs and the treatment of psychiatric disorders J.G. Hardman L.E. Limbird The Pharmacological Basis of Therapeutics 9th ed. 1996 McGraw-Hill New York 399 430
215. E. Romeo A. Ströhle G. Spalletta F. di Michele B. Hermann F. Holsboer A. Pasini R. Rupprecht Effects of antidepressant treatment on neuroactive steroids in major depression Am. J. Psychiatry 155 7 1998 910 913
216. V. Uzunova Y. Sheline J.M. Davis A. Rasmusson D.P. Uzunov E. Costa A. Guidottii Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine Proc. Natl Acad. Sci. USA 95 1998 3239 3244
217. R. Rupprecht F. Holsboer Neuroactive steroids: mechanism of action and neuropsychopharmacological perspectives Trends Neurosci. 22 1999 410 416
218. D.P. Uzunov T.B. Cooper E. Costa A. Guidotti Fluoxetine-elicited changes in brain neurosteroid content measured by negative ion mass fragmentography Proc. Natl Acad. Sci. USA 93 1996 12599 12604
219. A receptor Brain Res. 561 1 1991 157 161
220. A receptors J. Neuroendocrinol. 7 1995 171 177
221. S. Wieland N.C. Lan S. Mirasedeghi K.W. Gee Anxiolytic activity of the progesterone metabolite 5α-pregnan-3α-ol-20-one Brain Res. 565 1991 263 268
222. S. Wieland J.D. Belluzi L. Stein N.C. Lan Comparative behavioral characterization of the neuroactive steroids 3α-OH, 5α-pregnan-20-one and 3α-OH, 5β-pregnan-20-one in rodents Psychopharmacology 118 1995 65 71
223. S.M. Paul R.H. Purdy Neuroactive steroids FASEB J. 6 1992 2311 2322
224. M.J. Morrell Epilepsy in women: the science of why it is special Neurology 53 4 1999 S42 S48
225. T. Bäckström A. Cartensen Estrogen and progesterone in plasma in relation to premenstrual tension J. Steroid Biochem. 5 1974 257 260
226. D.M. Ball P. Glue S. Wilson D.J. Nutt Pharmacology of saccadic eye movements in man. 1. Effects of the benzodiazepine receptor ligands midazolam and flumazenil Psychopharmacology 105 1991 361 367
227. I. Sundström A. Andersson S. Nyberg D. Ashbrook R.H. Purdy T. Bäckström Patients with premenstrual syndrome have a different sensitivity to a neuroactive steroid during the menstrual cycle compared to control subjects Neuroendocrinology 67 2 1998 126 138
228. I. Sundström S. Nyberg T. Bäckström Patients with premenstrual syndrome have reduced sensitivity to midazolam compared to control subjects Neuropsychopharmacology 17 6 1997 370 381
229. I. Sundström D. Ashbrook T. Bäckström Reduced benzodiazepine sensitivity in patients with premenstrual syndrome: a pilot study Psychoneuroendocrinology 22 1 1997 25 38
230. M.A. Gallo S.S. Smith 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
231. P.J. Schmidt R.H. Purdy P.H. Moore Jr S.M. Paul D.R. Rubinow Circulating levels of anxiolytic steroids in the luteal phase in women with premenstrual syndrome and in control subjects J. Clin. Endocrinol. Metab. 79 1994 1256 1260
232. M. Wang L. Seippel R.H. Purdy T. Bäckström Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5α-pregnane-3,20-dione and 3α-hydroxy-5α-pregnan-20-one J. Clin. Endocrinol. Metab. 81 3 1996 1076 1082
233. A.J. Rapkin M. Morgan L. Goldman D.W. Brann D. Simone V.B. Mahesh Progesterone metabolite allopregnanolone in women with premenstrual syndrome Obstet. Gynecol. 90 5 1997 709 714
234. A.G. Herzog P. Klein E.J. Rensil Three patterns of catamenial epilepsy Epilepsia 38 1997 1082 1088
235. D.S. Reddy M.A. Rogawski Enhanced anticonvulsant activity of ganaxolone after neurosteroid withdrawal in a rat model of catamenial epilepsy J. Pharmacol. Exp. Ther. 294 3 2000 909 915
236. M.H. Moran S.S. Smith Progesterone withdrawal I: pro-convulsant effects Brain Res. 807 1–2 1998 84 90
237. T.G. Kokate M.K. Banks T. Magee S. Yamaguchi M.A. Rogawski Finasteride, a 5α-reductase inhibitor, blocks the anticonvulsant activity of progesterone in mice J. Pharmacol. Exp. Ther. 288 2 1999 679 684
238. M. Gasior R.B. Carter S.R. Goldberg J.M. Witkin Anticonvulsant and behavioral effects of neuroactive steroids alone and in conjunction with diazepam J. Pharmacol. Exp. Ther. 282 1997 543 553
239. A receptor J. Pharmacol. Exp. Ther. 280 1997 1284 1295
240. M. Gasior R.B. Carter J.M. Witkin Neuroactive steroids: potential therapeutic use in neurological and psychiatric disorders Trends Pharmacol. Sci. 20 1999 107 112
241. D. Belelli M.B. Bolger K.W. Gee Anticonvulsant profile of the progesterone metabolite 5α-pregnan-3α-ol-20-one Eur. J. Pharmacol. 166 1989 325 329
242. M. Beekman J.T. Ungard M. Gasior R.B. Carter D. Dijkstra S.R. Goldberg J.M. Witkin Reversal of behavioral effects of pentylenetetrazol by the neuroactive steroid ganaloxone J. Pharmacol. Exp. Ther. 284 1998 868 877
243. E.P. Monaghan L.A. Navalta L. Shum D.W. Ashbrook D.A. Lee Initial human experience with ganaxolone, a neuroactive steroid with antiepileptic activity Epilepsia 38 9 1997 1026 1031
244. A. Araque R.P. Parpura R.P. Sanzgiri P.G. Haydon Tripartite synapses: glia, the unacknowledged partner Trends Neurosci. 22 1999 208 215
245. D.T. Theodosis B. MacVicar Neurone–glial interactions in the hypothalamus and pituitary Trends Neurosci. 19 1996 363 367
246. C.L. Jordan Glia as mediators of steroid hormone action on the nervous system: an overview J. Neurobiol. 40 1999 434 445