Modulation of steroidal levels by adrenalectomy/castration and inhibition of neurosteroid synthesis enzymes affect σ1 receptor-mediated behaviour in mice

European Journal of Neuroscience

Volumn 11, Issue 7, 1999, Pages 2385-2396

  Phan, V L ^a   Su, T P ^a   Privat, A ^a   Maurice, T ^a  

^a INSTITUT CHARLES GERHARDT   (France)

Author keywords

Finasteride; Learning and memory; Neurosteroids; Passive avoidance; Sigma1 receptor; Spontaneous alternation; Trilostane

Indexed keywords

4 AMINOBUTYRIC ACID; 5ALPHA PREGNANE 3,20 DIONE; ASPARTIC ACID; DIZOCILPINE; ENZYME; FINASTERIDE; N ALLYLNORMETAZOCINE; NEUROSTEROID; OXIDOREDUCTASE; PREGNENOLONE; PROGESTERONE; RECEPTOR; SIGMA OPIATE RECEPTOR; STEROID; TRILOSTANE; TRITIUM;

ADRENALECTOMY; AGING; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION CORTEX; BEHAVIOR; CASTRATION; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; IN VIVO STUDY; LEARNING; LEARNING DISORDER; MALE; MEMORY; MOUSE; NEUROMODULATION; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; STEROIDOGENESIS;

EID: 0032969123     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00656.x     Document Type: Article

References (79)

1. Baulieu, E.E. & Robel, P. 1996 Dehydroepiandrosterone and dehydro‐ epiandrosterone sulfate as neuroactive neurosteroids. J. Endocrinol., 150, S221 S239.
2. Baulieu, E.E. & Robel, P. 1998 Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids. Proc. Natl Acad. Sci. USA, 95, 4089 4091.
3. Bergeron, R., De Montigny, C., Debonnel, G. 1996 Potentiation of neuronal NMDA response induced by dehydroepiandrosterone and its suppression by progesterone: effects mediated via σ receptors. J. Neurosci., 16, 1193 1202.
4. Bouchard, P., Dumont, Y., Fournier, A., St.‐Pierre, S., Quirion, R. 1993 Evidence for in vivo interactions between neuropeptide Y‐related peptides and σ receptors in the mouse hippocampal formation. J. Neurosci., 13, 3926 3931.
5. Bowlby, M.R. 1993 Pregnenolone sulfate potentiation of N ‐methyl‐ d‐aspartate receptor channels in hippocampal neurons. Mol. Pharmacol., 43, 813 819.
6. Bradford, M.M. 1976 A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein‐dye binding. Anal. Biochem., 72, 248 254.
7. Cheney, D.L., Uzunov, D., Guidotti, A. 1995 Pregnenolone sulfate antagonizes dizocilpine amnesia: role for allopregnanolone. Neuroreport, 6, 1697 1700.
8. Compagnone, N.A. & Mellon, S.H. 1998 Dehydroepiandrosterone: a potential signalling molecule for neocortical organization during development. Proc. Natl Acad. Sci. USA, 95, 4678 4683.
9. Corpéchot, C., Robel, P., Axelson, M., Sjovall, J., Baulieu, E.E. 1981 Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc. Natl Acad. Sci. USA, 78, 4704 4707.
10. Corpéchot, C., Young, J., Calvel, M., Wehrey, C., Veltz, J.N., Touyer, G., Mouren, M., Prasad, V.V., Banner, C., Sjovall, J et al. 1993 Neurosteroids: 3α‐hydroxy‐5α‐pregnan‐20‐one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology, 133, 1003 1009.
11. Earley, B., Burke, M., Leonard, B.E., Gouret, C.J., Junien, J.L. 1991 Evidence for an anti‐amnesic effect of JO1784 in the rat: a potent and selective ligand for the σ receptor. Brain Res., 546, 282 286.
12. Flood, J.F., Morley, J.E., Roberts, E. 1992 Memory‐enhancing effects in male mice of pregnenolone and steroids metabolically derived from it. Proc. Natl Acad. Sci. USA, 89, 1567 1571.
13. Flood, J.F. & Roberts, E. 1988 Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res., 448, 178 181.
14. Guennoun, R., Fiddes, R.J., Gouezou, M., Lombes, M., Baulieu, E.E. 1995 A key enzyme in the biosynthesis of neurosteroids, 3β‐hydroxysteroid dehydrogenase/Δ5‐Δ4‐isomerase (3β‐HSD), is expressed in rat brain. Molec. Brain Res., 30, 287 300.
15. Guennoun, R., Schumacher, M., Robert, F., Delespierre, B., Gouezou, M., Eychenne, B., Akwa, Y., Robel, P., Baulieu, E.E. 1997 Neurosteroids: expression of functional 3β‐hydroxysteroid dehydrogenase by rat sensory neurons and Schwann cells. Eur. J. Neurosci., 9, 2236 2247.
16. Hanner, M., Moebius, F.F., Flandorfer, A., Knaus, H.G., Striessnig, J., Kempner, E., Glossmann, H. 1996 Purification, molecular cloning, and expression of the mammalian σ 1 ‐binding site. Proc. Natl Acad. Sci. USA, 93, 8072 8077.
17. Irwin, R.P., Lin, S.Z., Rogawski, M.A., Purdy, R.H., Paul, S.M. 1994 Steroid potentiation and inhibition of N ‐methyl‐ d‐aspartate receptor‐mediated intracellular Ca ++ responses: structure‐activity studies. J. Pharmacol. Exp. Ther., 271, 677 682.
18. Irwin, R.P., Maragakis, N.J., Rogawski, M.A., Purdy, R.H., Farb, D.H., Paul, S.M. 1992 Pregnenolone sulfate augments NMDA receptor mediated increases in intracellular Ca 2+ in cultured rat hippocampal neurons. Neurosci. Lett., 141, 30 34.
19. Itoh, J., Nabeshima, T., Kameyama, T. 1990 Utility of an elevated plus‐maze for the evaluation of memory in mice: effects of nootropics, scopolamine and electroconvulsive shock. Psychopharmacology (Berl.), 101, 27 33.
20. Kamei, H., Kameyama, T., Nabeshima, T. 1996a (+) ‐SKF‐10,047 and dextromethorphan ameliorate conditioned fear stress through the activation of phenytoin‐regulated σ 1 sites. Eur. J. Pharmacol., 299, 21 28.
21. Kamei, H., Kameyama, T., Nabeshima, T. 1996b (+) ‐SKF‐10,047 and dextromethorphan ameliorate conditioned fear stress via dopaminergic systems linked to phenytoin‐regulated σ 1 sites. Eur. J. Pharmacol., 309, 149 158.
22. Kekuda, R., Prasad, P.D., Fei, Y.J., Leibach, F.H., Ganapathy, V. 1996 Cloning and functional expression of the human type 1σ receptor (hSigmaR1). Biochem. Biophys. Res. Commun., 229, 553 558.
23. Klein, M., Cooper, T.B., Musacchio, J.M. 1994 Effects of haloperidol and reduced haloperidol on binding to σ sites. Eur. J. Pharmacol., 254, 239 248.
24. Klein, M. & Musacchio, J.M. 1994 Effects of cytochrome P‐450 ligands on the binding of [ 3 H]dextrometorphan and sigma ligands to guinea‐pig brain. In: Itzhack, I, ed. Sigma Receptors. Academic Press, San Diego, CA, pp. 243 262.
25. Ladle, D.R., Jacobson, N.A., Lephart, E.D. 1997 Hypothalamic aromatase cytochrome P450 and 5α‐reductase enzyme activities in pregnant and female rats. Life Sci., 61, 2017 2026.
26. Lephart, E.D., Andersson, S., Simpson, E.R. 1990 Expression of neural 5 α‐reductase messenger ribonucleic acid: comparison to 5α‐reductase activity during prenatal development in the rat. Endocrinology, 127, 1121 1128.
27. Maione, S., Berrino, L., Vitagliano, S., Leyva, J., Rossi, F. 1992 Pregnenolone sulfate increases the convulsant potency of N ‐methyl‐ d‐aspartate in mice. Eur. J. Pharmacol., 219, 477 479.
28. Majewska, M.D., Harrison, N.L., Schwartz, R.D., Barker, J.L., Paul, S.M. 1986 Steroid hormone metabolites are barbiturate‐like modulators of the GABA receptor. Sci., 232, 1004 1007.
29. Mathis, C., Paul, S.M., Crawley, J.N. 1994 The neurosteroid pregnenolone sulfate blocks NMDA antagonist‐induced deficits in a passive avoidance memory task. Psychopharmacology (Berl.), 116, 201 206.
30. Matsuno, K., Kobayashi, T., Tanaka, M.K., Mita, S. 1996 σ 1 receptor subtype is involved in the relief of behavioral despair in the mouse forced swimming test. Eur. J. Pharmacol., 312, 267 271.
31. Matsuno, K., Matsunaga, K., Mita, S. 1992 Increase of extracellular acetylcholine level in rat frontal cortex induced by (+) N ‐allylnormetazocine as measured by brain microdialysis. Brain Res., 575, 315 319.
32. Matsuno, K., Senda, T., Matsunaga, K., Mita, S. 1994 Ameliorating effects of sigma receptor ligands on the impairment of passive avoidance tasks in mice: involvement in the central acetylcholinergic system. Eur. J. Pharmacol., 261, 43 51.
33. Maurice, T., Hiramatsu, M., Itoh, J., Kameyama, T., Hasegawa, T., Nabeshima, T. 1994a Behavioral evidence for a modulating role of sigma ligands in memory processes. I. Attenuation of dizocilpine (MK‐801) ‐induced amnesia. Brain Res., 647, 44 56.
34. Maurice, T., Hiramatsu, M., Itoh, J., Kameyama, T., Hasegawa, T., Nabeshima, T. 1994b Low dose of 1,3‐di (2‐tolyl) guanidine (DTG) attenuates MK‐801‐induced spatial working memory impairment in mice. Psychopharmacology (Berl.), 114, 520 522.
35. Maurice, T., Hiramatsu, M., Kameyama, T., Hasegawa, T., Nabeshima, T. 1994c Behavioral evidence for a modulating role of sigma ligands in memory processes. II. Reversion of carbon monoxide‐induced amnesia. Brain Res., 647, 57 64.
36. Maurice, T., Junien, J.‐L., Privat, A. 1997 Dehydroepiandrosterone sulfate attenuates dizocilpine‐induced learning impairment in mice via σ 1 ‐receptors. Behav. Brain Res., 83, 159 164.
37. Maurice, T. & Lockhart, B.P. 1997 Neuroprotective and anti‐amnesic potentials of σ (sigma) receptor ligands. Prog. Neuropsychopharmacol. Biol. Psychiatr., 21, 69 102.
38. Maurice, T., Phan, V.L., Noda, Y., Yamada, K., Privat, A., Nabeshima, T. 1999 The attenuation of learning impairments induced after exposure to CO or trimethyltin in mice by sigma (σ) receptor involves both σ 1 and σ 2 sites. Br. J. Pharmacol., in press.
39. Maurice, T. & Privat, A. 1997 SA4503, a novel cognitive enhancer with σ 1 receptor agonist properties, facilitates NMDA receptor‐dependent learning in mice. Eur. J. Pharmacol., 328, 9 18.
40. Maurice, T., Roman, F.J., Privat, A. 1996a Modulation by neurosteroids of the in vivo (+) ‐[3H]SKF‐10,047 binding to σ 1 receptors in the mouse forebrain. J. Neurosci. Res., 46, 734 743.
41. Maurice, T., Roman, F.J., Su, T.‐P., Privat, A. 1996b Beneficial effects of sigma agonists on the age‐related learning impairment in the senescence‐accelerated mouse (SAM). Brain Res., 733, 219 230.
42. Maurice, T., Su, T.‐P., Parish, D.W., Nabeshima, T., Privat, A. 1994d PRE‐084, a sigma selective PCP derivative, attenuates MK‐801‐induced impairment of learning in mice. Pharmacol. Biochem. Behav., 49, 859 869.
43. Maurice, T., Su, T.‐P., Privat, A. 1998 Sigma 1 (σ 1) receptor agonists and neurosteroids attenuate β 25–35 ‐amyloid peptide‐induced amnesia in mice through a common mechanism. Neuroscience, 83, 413 428.
44. Mayo, W., Dellu, F., Robel, P., Cherkaoui, J., Le Moal, M., Baulieu, E.E., Simon, H. 1993 Infusion of neurosteroids into the nucleus basalis magnocellularis affects cognitive processes in the rat. Brain Res., 607, 324 328.
45. McCann, D.J. & Su, T.‐P. 1991 Solubilization and characterization of haloperidol‐sensitive (+) ‐[ 3 H]SKF‐10,047 binding sites (σ sites) from rat liver membranes. J. Pharmacol. Exp. Ther., 257, 547 554.
46. Moebius, F.F., Reiter, R.J., Hanner, M., Glossmann, H. 1997 High affinity of σ 1 ‐binding sites for sterol isomerization inhibitors: evidence for a pharmacological relationship with the yeast sterol C 8–C 7 isomerase. Br. J. Pharmacol., 121, 1 6.
47. Monnet, F.P., Blier, P., Debonnel, G., De Montigny, C. 1992a Modulation by sigma ligands of N ‐methyl‐ d‐aspartate‐induced [ 3 H]noradrenaline release in the rat hippocampus: G‐protein dependency. Naunyn Schmiedebergs Arch. Pharmacol., 346, 32 39.
48. Monnet, F.P., Debonnel, G., De Montigny, C. 1992b In vivo electrophysiological evidence for a selective modulation of N ‐methyl‐ d‐aspartate‐induced neuronal activation in rat CA3 dorsal hippocampus by sigma ligands. J. Pharmacol. Exp. Ther., 261, 123 130.
49. Monnet, F.P., Debonnel, G., Junien, J.L., De Montigny, C. 1990 N ‐methyl‐ d‐aspartate‐induced neuronal activation is selectively modulated by sigma receptors. Eur. J. Pharmacol., 179, 441 445.
50. Monnet, F.P., Mahe, V., Robel, P., Baulieu, E.E. 1995 Neurosteroids, via sigma receptors, modulate the [ 3 H]norepinephrine release evoked by N ‐methyl‐ d‐aspartate in the rat hippocampus. Proc. Natl Acad. Sci. USA, 92, 3774 3778.
51. Ohno, M. & Watanabe, S. 1995 Intrahippocampal administration of (+) ‐SKF‐10,047, a sigma ligand, reverses MK‐801‐induced impairment of working memory in rats. Brain Res., 684, 237 242.
52. Pan, Y.‐X., Mey, J., Xu, J., Wan, B.‐L., Zuckerman, A., Pasternak, G.W. 1998 Cloning and characterization of a mouse σ 1 receptor. J. Neurochem., 70, 2279 2285.
53. Paul, S.M. & Purdy, R.H. 1992 Neuroactive steroids. FASEB J., 6, 2311 2322.
54. Purdy, R.H., Morrow, A.L., Moore, P.H., Paul, S.M. 1991 Stress‐induced elevations of gamma‐aminobutyric acid type A receptor‐active steroids in the rat brain. Proc. Natl Acad. Sci. USA, 88, 4553 4557.
55. Quirion, R., Bowen, W.D., Itzhak, Y., Junien, J.L., Musacchio, J.M., Rothman, R.B., Su, T.P., Tam, S.W., Taylor, D.P. 1992 A proposal for the classification of sigma binding sites. Trends Pharmacol. Sci., 13, 85 86.
56. Racagni, G., Apud, J.A., Cocchi, D., Locatelli, V., Muller, E.E. 1982 GABAergic control of anterior pituitary hormone secretion. Life Sci., 31, 823 838.
57. Rhodes, M.E., Li, P.K., Flood, J.F., Johnson, D.A. 1996 Enhancement of hippocampal acetylcholine release by the neurosteroid dehydroepiandrosterone sulfate: an in vivo microdialysis study. Brain Res., 733, 284 286.
58. Roberts, E., Bologa, L., Flood, J.F., Smith, G.E. 1987 Effects of dehydroepiandrosterone and its sulfate on brain tissue in culture and on memory in mice. Brain Res., 406, 357 362.
59. Roman, F.J., Pascaud, X., Duffy, O., Junien, J.L. 1991 N ‐methyl‐ d ‐aspartate receptor complex modulation by neuropeptide Y and peptide YY in rat hippocampus in vitro. Neurosci. Lett., 122, 202 204.
60. Romeo, E., Cheney, D.L., Zivkovic, I., Costa, E., Guidotti, A. 1994 Mitochondrial diazepam‐binding inhibitor receptor complex agonists antagonize dizocilpine amnesia: putative role for allopregnanolone. J. Pharmacol. Exp. Ther., 270, 89 96.
61. Schumacher, M., Guennoun, R., Robel, P., Baulieu, E.E. 1997 Neurosteroids in the Hippocampus. Neuronal Plasticity Memory. Stress, 2, 65 78.
62. Seth, P., Fei, Y.J., Li, H.W., Huang, W., Leibach, F.H., Ganapathy, V. 1998 Cloning and functional characterization of a σ receptor from rat brain. J. Neurochem., 70, 922 931.
63. Seth, P., Leibach, F.H., Ganapathy, V. 1997 Cloning and structural analysis of the cDNA and the gene encoding the murine type 1 sigma receptor. Biochem. Biophys. Res. Commun., 241, 535 540.
64. Siniscalchi, A., Cristofori, P., Veratti, E. 1987 Influence of N ‐allyl‐normetazocine on acetylcholine release from brain slices: involvement of muscarinic receptors. Naunyn Schmiedebergs Arch. Pharmacol., 336, 425 429.
65. Su, T.‐P.,. London, E., D., Jaffe, J.H. 1988 Steroid binding at σ receptors suggests a link between endocrine, nervous, and immune systems. Science, 240, 219 221.
66. Su, T.‐P., Hayashi, T., Maurice, T. 1998 G‐Protein‐linked l‐type Ca 2+ channels on plasma membranes and IP 3 receptors on endoplasmic reticulum in NG‐108 cells are regulated by σ 1 receptors: Ca 2+ mobilization and σ 1 receptor antisense studies. Soc. Neurosci. Abstract., 24, 2055.
67. Su, T.‐P. & Junien, J.‐L. 1994 Sigma Receptors in the Central Nervous System and the Periphery. In: Itzhak, Y, ed. Sigma Receptors, Academic Press, San Diego, pp. 21 44.
68. Su, T.P., Wu, X.Z., Cone, E.J., Shukla, K., Gund, T.M., Dodge, A.L., Parish, D.W. 1991 Sigma compounds derived from phencyclidine: identification of PRE‐084, a new, selective sigma ligand. J. Pharmacol. Exp. Ther., 259, 543 548.
69. Taylor, D.P. & Dekleva, J. 1987 Potential antipsychotic BMY‐14802 selectively binds to sigma sites. Drug Dev. Res., 11, 65 70.
70. Ujike, H., Okumura, K., Zushi, Y., Akiyama, K., Otsuki, S. 1992 Persistent supersensitivity of σ receptors develops during repeated methamphetamine treatment. Eur. J. Pharmacol., 211, 323 328.
71. Urani, A., Privat, A., Maurice, T. 1998 The modulation by neurosteroids of the scopolamine‐induced learning impairment in mice involves an interaction with sigma 1 (σ 1) receptors. Brain Res., 799, 64 77.
72. Vallée, M., Mayo, W., Darnaudery, M., Corpechot, C., Young, J., Koehl, M., Le Moal, M., Baulieu, E.E., Robel, P., Simon, H. 1997 Neurosteroids: deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus. Proc. Natl Acad. Sci. U S A, 94, 14865 14870.
73. Wakerley, J.B. & Richardson, C.M. 1997 The neurosteroid pregnenolone sulphate enhances NMDA‐induced phasic firing of vasopressin neurones in the rat supraoptic nucleus. Neurosci. Lett., 226, 123 126.
74. Walker, J.M., Bowen, W.D., Walker, F.O., Matsumoto, R.R., De Costa, B., Rice, K.C. 1990 Sigma receptors: biology and function. Pharmacol. Rev., 42, 355 402.
75. Wu, X.Z., Bell, J.A., Spivak, C.E.,. London, E., D., Su, T.P. 1991 Electrophysiological and binding studies on intact NCB‐20 cells suggest presence of a low affinity sigma receptor. J. Pharmacol. Exp. Ther., 257, 351 359.
76. Yamada, M., Nishigami, T., Nakasho, K., Nishimoto, Y., Miyaji, H. 1994 Relationship between sigma‐like site and progesterone‐binding site of adult male rat liver microsomes. Hepatology, 20, 1271 1280.
77. Young, J., Corpéchot, C., Haug, M., Gobaille, S., Baulieu, E.E., Robel, P. 1991 Suppressive effects of dehydroepiandrosterone and 3β‐methyl‐androst‐5‐en‐17‐one on attack towards lactating female intruders by castrated male mice. II. Brain neurosteroids. Biochem. Biophys. Res. Commun., 174, 892 897.
78. Young, J., Corpéchot, C., Perche, F., Eychenne, B., Haug, M., Baulieu, E.E., Robel, P. 1996 Neurosteroids in the mouse brain: behavioral and pharmacological effects of a 3β‐hydroxysteroid dehydrogenase inhibitor. Steroids, 61, 144 149.
79. Young, J., Corpéchot, C., Perché, F., Haug, M., Baulieu, E.E., Robel, P. 1994 Neurosteroids: pharmacological effects of a 3β‐hydroxysteroid dehydrogenase inhibitor. Endocrine, 2, 505 509.