Neurosteroid modulation of N-methyl-d-aspartate receptors: Molecular mechanism and behavioral effects

Steroids

Volumn 76, Issue 13, 2011, Pages 1409-1418

  Korinek, Miloslav ^a   Kapras, Vojtech ^b   Vyklicky, Vojtech ^a   Adamusova, Eva ^a   Borovska, Jirina ^a   Vales, Karel ^a   Stuchlik, Ales ^a   Horak, Martin ^a   Chodounska, Hana ^b   Vyklicky Jr , Ladislav ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

Glutamate receptor; Ion channel; N Methyl d aspartate receptor; Neurosteroid; Pregnanolone sulfate; Pregnenolone sulfate

Indexed keywords

11 KETO PREGNENOLONE SULFATE; 11BETA HYDROXY PREGNENOLONE SULFATE; 17 HYDROXY PREGNENOLONE SULFATE; 20 OXO 5ALAPHA PREGNAN 3ALPHA YL SULFATE; 20 OXO 5ALPHA PREGNAN 3ALPHA YL HEMISUCCINATE; 20 OXO 5ALPHA PREGNAN 3BETA YL SULFATE; 20 OXO 5ALPHA PREGNANE 3ALPHA,7ALPHA DIYL 3 HEMISUCCINATE 7 ACETATE; 20 OXO 5ALPHA PREGNANE 3ALPHA,7ALPHA DIYL 3 SULFATE 7 ACETATE; 20 OXO 5ALPHA PREGNANE 3ALPHA,7ALPHA DIYL 3 SULFATE 7 NICOTINATE; 20 OXO 5BETA PREGNAN 3ALPHA YL HEMIGLUTARATE; 20 OXO 5BETA PREGNAN 3ALPHA YL HEMIOXALATE; 20 OXO 5BETA PREGNAN 3ALPHA YL HEMISUCCINATE; 20 OXO 5BETA PREGNAN 3BETA YL SULFATE; 20 OXO 5BETA PREGNANE 3ALPHA,7ALPHA DIYL 3 HEMISUCCINATE 7 ACETATE; 20 OXO 5BETA PREGNANE 3ALPHA,7ALPHA DIYL 3 SULFATE 7 ACETATE; 20 OXO 5BETA PREGNANE 3ALPHA,7ALPHA DIYL 3 SULFATE 7 NICOTINATE; 20 OXO PREGN 5 EN 3BETA YL METHYL SUCCINATE; 20BETA DIHYDRO PREGNENOLONE SULFATE; 21 ACETOXY PREGNENOLONE SULFATE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 7 KETO PREGNENOLONE SULFATE; ELTANOLONE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROSTEROID; PREGNANOLONE FORMATE; PREGNANOLONE SULFATE; PREGNENOLONE 3BETA HEMIGLUTARATE; PREGNENOLONE 3BETA HEMIOXALATE; PREGNENOLONE 3BETA HEMISUCCINATE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ALLOSTERISM; BEHAVIOR DISORDER; CENTRAL NERVOUS SYSTEM DISEASE; CONCENTRATION RESPONSE; DRUG MECHANISM; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG SYNTHESIS; HUMAN; NEUROPROTECTION; NONHUMAN; REVIEW; STRESS;

ANIMALS; BEHAVIOR; DISEASE; HUMANS; NEUROTRANSMITTER AGENTS; RECEPTORS, GABA; RECEPTORS, N-METHYL-D-ASPARTATE; STEROIDS;

ANIMALIA; VERTEBRATA;

EID: 80053576102     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2011.09.002     Document Type: Review

References (107)

1. N.J. McKenna, R.B. Lanz, and B.W. O'Malley Nuclear receptor coregulators: cellular and molecular biology Endocr Rev 20 1999 321 344 (Pubitemid 30649811)
2. E.E. Baulieu, and P. Robel Neurosteroids: a new brain function? J Steroid Biochem Mol Biol 37 1990 395 403
3. H. Selye Anesthetic effect of steroid hormones Proc Soc Exp Biol Med 46 1941 116 121
4. A.M. VanDongen Biology of the NMDA receptor 2009 CRC Press Boca Raton
5. R. Dingledine, K. Borges, D. Bowie, and S.F. Traynelis The glutamate receptor ion channels Pharmacol Rev 51 1999 7 61 (Pubitemid 29113865)
6. A.I. Sobolevsky, M.P. Rosconi, and E. Gouaux X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462 2009 745 756
7. P. Paoletti Molecular basis of NMDA receptor functional diversity Eur J Neurosci 33 2011 1351 1365
8. M.H. Ulbrich, and E.Y. Isacoff Subunit counting in membrane-bound proteins Nat Methods 4 2007 319 321 (Pubitemid 46766975)
9. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540 (Pubitemid 24100885)
10. H. Monyer, R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, and H. Lomeli Heteromeric NMDA receptors: molecular and functional distinction of subtypes Science 256 1992 1217 1221
11. S. Cull-Candy, S. Brickley, and M. Farrant NMDA receptor subunits: diversity, development and disease Curr Opin Neurobiol 11 2001 327 335 (Pubitemid 32524098)
12. M. Sheng, J. Cummings, L.A. Roldan, Y.N. Jan, and L.Y. Jan Changing subunit composition of heteromeric NMDA receptors during development of rat cortex Nature 368 1994 144 147 (Pubitemid 24101524)
13. T.R. Tolle, A. Berthele, W. Zieglgansberger, P.H. Seeburg, and W. Wisden The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray J Neurosci 13 1993 5009 5028 (Pubitemid 24000990)
14. C.G. Thomas, J.J. Krupp, E.E. Bagley, R. Bauzon, S.F. Heinemann, and B. Vissel Probing N-methyl-d-aspartate receptor desensitization with the substituted-cysteine accessibility method Mol Pharmacol 69 2006 1296 1303
15. N.W. Kleckner, and R. Dingledine Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes Science 241 1988 835 837
16. J.W. Johnson, and P. Ascher Glycine potentiates the NMDA response in cultured mouse brain neurons Nature 325 1987 529 531 (Pubitemid 17056733)
17. H. Furukawa, S.K. Singh, R. Mancusso, and E. Gouaux Subunit arrangement and function in NMDA receptors Nature 438 2005 185 192 (Pubitemid 41599865)
18. J.E. Chatterton, M. Awobuluyi, L.S. Premkumar, H. Takahashi, M. Talantova, and Y. Shin Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits Nature 415 2002 793 798 (Pubitemid 34150501)
19. C.T. Smothers, and J.J. Woodward Pharmacological characterization of glycine-activated currents in HEK 293 cells expressing N-methyl-d-aspartate NR1 and NR3 subunits J Pharmacol Exp Ther 322 2007 739 748 (Pubitemid 47105819)
20. S.F. Traynelis, L.P. Wollmuth, C.J. McBain, F.S. Menniti, K.M. Vance, and K.K. Ogden Glutamate receptor ion channels: structure, regulation, and function Pharmacol Rev 62 2010 405 496
21. B. Feng, R.M. Morley, D.E. Jane, and D.T. Monaghan The effect of competitive antagonist chain length on NMDA receptor subunit selectivity Neuropharmacology 48 2005 354 359 (Pubitemid 40249998)
22. J.A. Kemp, A.C. Foster, P.D. Leeson, T. Priestley, R. Tridgett, and L.L. Iversen 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of the N-methyl-d-aspartate receptor complex Proc Natl Acad Sci USA 85 1988 6547 6550
23. P. Ascher, and L. Nowak The role of divalent cations in the N-methyl-d-aspartate responses of mouse central neurones in culture J Physiol Lond 399 1988 247 266
24. M. Park-Chung, A. Malayev, R.H. Purdy, T.T. Gibbs, and D.H. Farb Sulfated and unsulfated steroids modulate gamma-aminobutyric acid A receptor function through distinct sites Brain Res 830 1999 72 87 (Pubitemid 29251714)
25. M. Park-Chung, F.S. Wu, and D.H. Farb 3 alpha-Hydroxy-5 beta-pregnan-20-one sulfate: a negative modulator of the NMDA-induced current in cultured neurons Mol Pharmacol 46 1994 146 150
26. A. Malayev, T.T. Gibbs, and D.H. Farb Inhibition of the NMDA response by pregnenolone sulphate reveals subtype selective modulation of NMDA receptors by sulphated steroids Br J Pharmacol 135 2002 901 909 (Pubitemid 34214448)
27. M. Petrovic, M. Sedlacek, M. Horak, H. Chodounska, and L. Vyklicky Jr. 20-Oxo-5beta-pregnan-3alpha-yl sulfate is a use-dependent NMDA receptor inhibitor J Neurosci 25 2005 8439 8450 (Pubitemid 41324730)
28. M.L. Mayer, G.L. Westbrook, and P.B. Guthrie Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones Nature 309 1984 261 263 (Pubitemid 14139936)
29. L. Nowak, P. Bregestovski, P. Ascher, A. Herbet, and A. Prochiantz Magnesium gates glutamate-activated channels in mouse central neurones Nature 307 1984 462 465 (Pubitemid 14132062)
30. J. Bormann Memantine is a potent blocker of N-methyl-d-aspartate (NMDA) receptor channels Eur J Pharmacol 166 1989 591 592 (Pubitemid 19195356)
31. C.R. Honey, Z. Miljkovic, and J.F. MacDonald Ketamine and phencyclidine cause a voltage-dependent block of responses to l-aspartic acid Neurosci Lett 61 1985 135 139 (Pubitemid 16201138)
32. C.L. Kussius, N. Kaur, and G.K. Popescu Pregnanolone sulfate promotes desensitization of activated NMDA receptors J Neurosci 29 2009 6819 6827
33. M. Park-Chung, F.S. Wu, R.H. Purdy, A.A. Malayev, T.T. Gibbs, and D.H. Farb Distinct sites for inverse modulation of N-methyl-d-aspartate receptors by sulfated steroids Mol Pharmacol 52 1997 1113 1123 (Pubitemid 28013731)
34. C.E. Weaver, M.B. Land, R.H. Purdy, K.G. Richards, T.T. Gibbs, and D.H. Farb Geometry and charge determine pharmacological effects of steroids on N-methyl-d-aspartate receptor-induced Ca(2+) accumulation and cell death J Pharmacol Exp Ther 293 2000 747 754 (Pubitemid 30417838)
35. T.T. Gibbs, S.J. Russek, and D.H. Farb Sulfated steroids as endogenous neuromodulators Pharmacol Biochem Behav 84 2006 555 567 (Pubitemid 350061235)
36. L. Stoll, J. Hall, N. Van Buren, A. Hall, L. Knight, and A. Morgan Differential regulation of ionotropic glutamate receptors Biophys J 92 2007 1343 1349 (Pubitemid 46203195)
37. G. Abdrachmanova, H. Chodounska, and L. Vyklicky Jr. Effects of steroids on NMDA receptors and excitatory synaptic transmission in neonatal motoneurons in rat spinal cord slices Eur J Neurosci 14 2001 495 502 (Pubitemid 34203457)
38. S. Weill-Engerer, J.P. David, V. Sazdovitch, P. Liere, B. Eychenne, and A. Pianos Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients J Clin Endocrinol Metab 87 2002 5138 5143 (Pubitemid 35316357)
39. F.S. Wu, T.T. Gibbs, and D.H. Farb Pregnenolone sulfate: a positive allosteric modulator at the N-methyl-d-aspartate receptor Mol Pharmacol 40 1991 333 336
40. M.R. Bowlby Pregnenolone sulfate potentiation of N-methyl-d-aspartate receptor channels in hippocampal neurons Mol Pharmacol 43 1993 813 819 (Pubitemid 23146282)
41. M. Ceccon, G. Rumbaugh, and S. Vicini Distinct effect of pregnenolone sulfate on NMDA receptor subtypes Neuropharmacology 40 2001 491 500 (Pubitemid 32209034)
42. M. Horak, K. Vlcek, M. Petrovic, H. Chodounska, and L. Vyklicky Jr. Molecular mechanism of pregnenolone sulfate action at NR1/NR2B receptors J Neurosci 24 2004 10318 10325 (Pubitemid 39552615)
43. M. Horak, K. Vlcek, H. Chodounska, and L. Vyklicky Jr. Subtype-dependence of N-methyl-d-aspartate receptor modulation by pregnenolone sulfate Neuroscience 137 2006 93 102 (Pubitemid 43031477)
44. M.K. Jang, D.F. Mierke, S.J. Russek, and D.H. Farb A steroid modulatory domain on NR2B controls N-methyl-d-aspartate receptor proton sensitivity Proc Natl Acad Sci USA 101 2004 8198 8203 (Pubitemid 38698077)
45. N.J. Leidenheimer, and R. Chapell Effects of PKC activation and receptor desensitization on neurosteroid modulation of GABA(A) receptors Brain Res Mol Brain Res 52 1997 173 181 (Pubitemid 28043460)
46. A. Fancsik, D.M. Linn, and J.G. Tasker Neurosteroid modulation of GABA IPSCs is phosphorylation dependent J Neurosci 20 2000 3067 3075 (Pubitemid 30263123)
47. M. Petrovic, M. Sedlacek, O. Cais, M. Horak, H. Chodounska, and L. Vyklicky Jr. Pregnenolone sulfate modulation of N-methyl-d-aspartate receptors is phosphorylation dependent Neuroscience 160 2009 616 628
48. L.D. Partridge, and C.F. Valenzuela Neurosteroid-induced enhancement of glutamate transmission in rat hippocampal slices Neurosci Lett 301 2001 103 106 (Pubitemid 32206696)
49. L. Chen, and M. Sokabe Presynaptic modulation of synaptic transmission by pregnenolone sulfate as studied by optical recordings J Neurophysiol 94 2005 4131 4144 (Pubitemid 41691774)
50. D.A. Meyer, M. Carta, L.D. Partridge, D.F. Covey, and C.F. Valenzuela Neurosteroids enhance spontaneous glutamate release in hippocampal neurons J Biol Chem 277 2002 28725 28732
51. T. Johansson, P.A. Frandberg, F. Nyberg, and P. Le Greves Molecular mechanisms for nanomolar concentrations of neurosteroids at NR1/NR2B receptors J Pharmacol Exp Ther 324 2008 759 768 (Pubitemid 351185871)
52. M. Elfverson, A.M. Linde, P. Le Greves, Q. Zhou, F. Nyberg, and T. Johansson Neurosteroids allosterically modulate the ion pore of the NMDA receptor consisting of NR1/NR2B but not NR1/NR2A Biochem Biophys Res Commun 372 2008 305 308
53. J.M. Torres, and E. Ortega DHEA, PREG and their sulphate derivatives on plasma and brain after CRH and ACTH administration Neurochem Res 28 2003 1187 1191 (Pubitemid 36734550)
54. P. Porcu, T.K. O'Buckley, S.E. Alward, C.E. Marx, L.J. Shampine, and S.S. Girdler Simultaneous quantification of GABAergic 3alpha,5alpha/3alpha,5beta neuroactive steroids in human and rat serum Steroids 74 2009 463 473
55. V. Uzunova, Y. Sheline, J.M. Davis, A. Rasmusson, D.P. Uzunov, and E. Costa 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 (Pubitemid 28135886)
56. C.E. Marx, R.D. Stevens, L.J. Shampine, V. Uzunova, W.T. Trost, and M.I. Butterfield Neuroactive steroids are altered in schizophrenia and bipolar disorder: relevance to pathophysiology and therapeutics Neuropsychopharmacology 31 2006 1249 1263 (Pubitemid 43971841)
57. Y. Wang, and W.J. Griffiths Capillary liquid chromatography combined with tandem mass spectrometry for the study of neurosteroids and oxysterols in brain Neurochem Int 52 2008 506 521
58. C. Corpechot, M. Synguelakis, S. Talha, M. Axelson, J. Sjovall, and R. Vihko Pregnenolone and its sulfate ester in the rat brain Brain Res 270 1983 119 125 (Pubitemid 13060692)
59. T. Higashi, Y. Daifu, T. Ikeshima, T. Yagi, and K. Shimada Studies on neurosteroids XV. Development of enzyme-linked immunosorbent assay for examining whether pregnenolone sulfate is a veritable neurosteroid J Pharm Biomed Anal 30 2003 1907 1917 (Pubitemid 35453995)
60. T. Higashi, H. Sugitani, T. Yagi, and K. Shimada Studies on neurosteroids XVI Levels of pregnenolone sulfate in rat brains determined by enzyme-linked immunosorbent assay not requiring solvolysis Biol Pharm Bull 26 2003 709 711 (Pubitemid 39663568)
61. P. Liere, A. Pianos, B. Eychenne, A. Cambourg, S. Liu, and W. Griffiths Novel lipoidal derivatives of pregnenolone and dehydroepiandrosterone and absence of their sulfated counterparts in rodent brain J Lipid Res 45 2004 2287 2302 (Pubitemid 39602976)
62. S. Liu, J. Sjovall, and W.J. Griffiths Neurosteroids in rat brain: extraction, isolation, and analysis by nanoscale liquid chromatography- electrospray mass spectrometry Anal Chem 75 2003 5835 5846 (Pubitemid 37356465)
63. M.J. Ebner, D.I. Corol, H. Havlikova, J.W. Honour, and J.P. Fry Identification of neuroactive steroids and their precursors and metabolites in adult male rat brain Endocrinology 147 2006 179 190 (Pubitemid 43004272)
64. M. Schumacher, P. Liere, Y. Akwa, K. Rajkowski, W. Griffiths, and K. Bodin Pregnenolone sulfate in the brain: a controversial neurosteroid Neurochem Int 52 2008 522 540
65. P. Liere, A. Pianos, B. Eychenne, A. Cambourg, K. Bodin, and W. Griffiths Analysis of pregnenolone and dehydroepiandrosterone in rodent brain: cholesterol autoxidation is the key J Lipid Res 50 2009 2430 2444
66. A. Lanthier, and 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 1986 445 449 (Pubitemid 17182431)
67. M. Mameli, M. Carta, L.D. Partridge, and C.F. Valenzuela Neurosteroid-induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors J Neurosci 25 2005 2285 2294 (Pubitemid 40322269)
68. N. Yaghoubi, A. Malayev, S.J. Russek, T.T. Gibbs, and D.H. Farb Neurosteroid modulation of recombinant ionotropic glutamate receptors Brain Res 803 1998 153 160 (Pubitemid 28392141)
69. J. Klak, M. Hill, A. Parizek, H. Havlikova, M. Bicikova, and R. Hampl Pregnanolone isomers, pregnenolone and their polar conjugates around parturition Physiol Res 52 2003 211 221 (Pubitemid 36427824)
70. E. Stastna, H. Chodounska, V. Pouzar, V. Kapras, J. Borovska, and O. Cais Synthesis of C3, C5, and C7 pregnane derivatives and their effect on NMDA receptor responses in cultured rat hippocampal neurons Steroids 74 2009 256 263
71. C.E. Weaver Jr., P. Marek, M. Park-Chung, S.W. Tam, and D.H. Farb Neuroprotective activity of a new class of steroidal inhibitors of the N-methyl-d-aspartate receptor Proc Natl Acad Sci USA 94 1997 10450 10454 (Pubitemid 27407062)
72. C. Wang, C.E. Marx, A.L. Morrow, W.A. Wilson, and S.D. Moore Neurosteroid modulation of GABAergic neurotransmission in the central amygdala: a role for NMDA receptors Neurosci Lett 415 2007 118 123 (Pubitemid 46386326)
73. C.E. Weaver, M. ParkChung, T.T. Gibbs, and D.H. Farb 17 Beta-estradiol protects against NMDA-induced excytotoxicity by direct inhibition of NMDA receptors Brain Res 761 1997 338 341 (Pubitemid 27305996)
74. M.D. Majewska, N.L. Harrison, R.D. Schwartz, J.L. Barker, and S.M. Paul Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor Science 232 1986 1004 1007 (Pubitemid 16085410)
75. A.M. Hosie, M.E. Wilkins, H.M. da Silva, and T.G. Smart Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites Nature 444 2006 486 489 (Pubitemid 44809065)
76. T.G. Kokate, B.E. Svensson, and M.A. Rogawski Anticonvulsant activity of neurosteroids: correlation with gamma-aminobutyric acid-evoked chloride current potentiation J Pharmacol Exp Ther 270 1994 1223 1229 (Pubitemid 24315243)
77. M. Wang, Y. He, L.N. Eisenman, C. Fields, C.M. Zeng, and J. Mathews 3Beta-hydroxypregnane steroids are pregnenolone sulfate-like GABA(A) receptor antagonists J Neurosci 22 2002 3366 3375 (Pubitemid 37465742)
78. K.D. Morris, and J. Amin Insight into the mechanism of action of neuroactive steroids Mol Pharmacol 66 2004 56 69 (Pubitemid 38822087)
79. S. Mennerick, Y. He, X. Jiang, B.D. Manion, M. Wang, and A. Shute Selective antagonism of 5alpha-reduced neurosteroid effects at GABA(A) receptors Mol Pharmacol 65 2004 1191 1197 (Pubitemid 38543489)
80. A.M. Hosie, M.E. Wilkins, and T.G. Smart Neurosteroid binding sites on GABA(A) receptors Pharmacol Ther 116 2007 7 19 (Pubitemid 47398919)
81. A.M. Hosie, L. Clarke, H. da Silva, and T.G. Smart Conserved site for neurosteroid modulation of GABA A receptors Neuropharmacology 56 2009 149 154
82. G. Akk, J. Bracamontes, and J.H. Steinbach Pregnenolone sulfate block of GABAA receptors: mechanism and involvement of a residue in the M2 region of the alpha subunit J Physiol 532 2001 673 684 (Pubitemid 32427883)
83. M.D. Wang, M. Rahman, D. Zhu, and T. Backstrom Pregnenolone sulphate and Zn2+ inhibit recombinant rat GABA(A) receptor through different channel property Acta Physiol (Oxf) 188 2006 153 162 (Pubitemid 44622363)
84. M.D. Wang, M. Rahman, D. Zhu, I.M. Johansson, and T. Backstrom 3Beta-hydroxysteroids and pregnenolone sulfate inhibit recombinant rat GABA(A) receptor through different channel property Eur J Pharmacol 557 2007 124 131 (Pubitemid 46186297)
85. B. Wardell, P.S. Marik, D. Piper, T. Rutar, E.M. Jorgensen, and B.A. Bamber Residues in the first transmembrane domain of the Caenorhabditis elegans GABA(A) receptor confer sensitivity to the neurosteroid pregnenolone sulfate Br J Pharmacol 148 2006 162 172 (Pubitemid 43873035)
86. R.M. Woodward, L. Polenzani, and R. Miledi Effects of steroids on gamma-aminobutyric acid receptors expressed in Xenopus oocytes by poly(A)+ RNA from mammalian brain and retina Mol Pharmacol 41 1992 89 103
87. S.R. Engel, and K.A. Grant Neurosteroids and behavior Int Rev Neurobiol 46 2001 321 348 (Pubitemid 33798726)
88. P.A. Lapchak The neuroactive steroid 3-alpha-ol-5-beta-pregnan-20-one hemisuccinate, a selective NMDA receptor antagonist improves behavioral performance following spinal cord ischemia Brain Res 997 2004 152 158 (Pubitemid 38058520)
89. G. Akk, D.F. Covey, A.S. Evers, J.H. Steinbach, C.F. Zorumski, and S. Mennerick Mechanisms of neurosteroid interactions with GABA(A) receptors Pharmacol Ther 116 2007 35 57 (Pubitemid 47391029)
90. B.O. Dubrovsky Steroids, neuroactive steroids and neurosteroids in psychopathology Prog Neuropsychopharmacol Biol Psychiatry 29 2005 169 192 (Pubitemid 40202904)
91. L. Rambousek, V. Bubenikova-Valesova, P. Kacer, K. Syslova, J. Kenney, and K. Holubova Cellular and behavioural effects of a new steroidal inhibitor of the N-methyl-d-aspartate receptor 3alpha5beta-pregnanolone glutamate Neuropharmacology 61 2011 61 68
92. Z. Li, R. Zhou, S. Cui, G. Xie, W. Cai, and M. Sokabe Dehydroepiandrosterone sulfate prevents ischemia-induced impairment of long-term potentiation in rat hippocampal CA1 by up-regulating tyrosine phosphorylation of NMDA receptor Neuropharmacology 51 2006 958 966 (Pubitemid 44528605)
93. D.A. Finn, A.J. Roberts, S. Long, M. Tanchuck, and T.J. Phillips Neurosteroid consumption has anxiolytic effects in mice Pharmacol Biochem Behav 76 2003 451 462 (Pubitemid 37487901)
94. J.Z. Tsien, P.T. Huerta, and S. Tonegawa The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory Cell 87 1996 1327 1338 (Pubitemid 27010115)
95. J.F. Flood, and E. Roberts Dehydroepiandrosterone sulfate improves memory in aging mice Brain Res 448 1988 178 181
96. R.L. Isaacson, J.A. Varner, J.M. Baars, and D. De Wied The effects of pregnenolone sulfate and ethylestrenol on retention of a passive avoidance task Brain Res 689 1995 79 84
97. M. Vallee, W. Mayo, M. Darnaudery, C. Corpechot, J. Young, and M. Koehl Neurosteroids: deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus Proc Natl Acad Sci USA 94 1997 14865 14870 (Pubitemid 28041466)
98. E. Martin-Garcia, and M. Pallares A post-training intrahippocampal anxiogenic dose of the neurosteroid pregnenolone sulfate impairs passive avoidance retention Exp Brain Res 191 2008 123 131
99. R. Citraro, E. Russo, S. Gratteri, E.D. Di Paola, G.F. Ibbadu, and C. Curinga Effects of non-competitive AMPA receptor antagonists injected into some brain areas of WAG/Rij rats, an animal model of generalized absence epilepsy Neuropharmacology 51 2006 1058 1067 (Pubitemid 44767582)
100. T.G. Kokate, K.N. Juhng, R.D. Kirkby, J. Llamas, S. Yamaguchi, and M.A. Rogawski Convulsant actions of the neurosteroid pregnenolone sulfate in mice Brain Res 831 1999 119 124 (Pubitemid 29336194)
101. M. Kavaliers, and D.M. Kinsella Male preference for the odors of estrous female mice is reduced by the neurosteroid pregnenolone sulfate Brain Res 682 1995 222 226
102. D.S. Reddy, and S.K. Kulkarni Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice Brain Res 752 1997 61 71 (Pubitemid 27143898)
103. N.I. Dubrovina, R.A. Tomilenko, and T.A. Obut Effects of dehydroepiandrosterone sulfate and dizocilpine on memory trace extinction in aggressive and submissive mice Zh Vyssh Nerv Deiat Im IP Pavlova 56 2006 684 690
104. O.T. Wolf, and C. Kirschbaum Dehydroepiandrosterone replacement in elderly individuals: still waiting for the proof of beneficial effects on mood or memory J Endocrinol Invest 22 1999 316 (Pubitemid 29224334)
105. O.M. Wolkowitz, V.I. Reus, E. Roberts, F. Manfredi, T. Chan, and S. Ormiston Antidepressant and cognition-enhancing effects of DHEA in major depression Ann NY Acad Sci 774 1995 337 339 (Pubitemid 26140392)
106. M. Bicikova, J. Tallova, M. Hill, Z. Krausova, and R. Hampl Serum concentrations of some neuroactive steroids in women suffering from mixed anxiety-depressive disorder Neurochem Res 25 2000 1623 1627 (Pubitemid 32052022)
107. C.E. Marx, R.S. Keefe, R.W. Buchanan, R.M. Hamer, J.D. Kilts, and D.W. Bradford Proof-of-concept trial with the neurosteroid pregnenolone targeting cognitive and negative symptoms in schizophrenia Neuropsychopharmacology 34 2009 1885 1903