The 3β-hydroxysteroid dehydrogenase inhibitor trilostane shows antidepressant properties in mice

Psychoneuroendocrinology

Volumn 34, Issue 5, 2009, Pages 644-659

  Espallergues, Julie ^a,b,c,d   Givalois, Laurent ^a,b,c   Temsamani, Jamal ^d   Laruelle, Claude ^d   Maurice, Tangui ^a,b,c  

^a UNIV MONTPELLIER   (France)

^b University of Montpellier   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d CLL Pharma   (France)

Author keywords

3 Hydroxysteroid dehydrogenase; Acute stress; Depression; Neuroactive steroids; Trilostane

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANTIDEPRESSANT AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; CORTICOTROPIN; TRILOSTANE; ANDROSTANOLONE; DRUG DERIVATIVE; MESSENGER RNA;

ADRENAL GLAND; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; DEPRESSION; DOSE RESPONSE; EXPLORATORY BEHAVIOR; FORCED SWIMMING TEST; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; IMMOBILIZATION STRESS; LOCOMOTION; MALE; MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; ORGAN WEIGHT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS; WEIGHT REDUCTION; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOTOR ACTIVITY; PSYCHOLOGIC TEST; SWIMMING;

3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; BEHAVIOR, ANIMAL; DEPRESSION; DIHYDROTESTOSTERONE; DRUG EVALUATION, PRECLINICAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; MICE; MODELS, BIOLOGICAL; MOTOR ACTIVITY; PSYCHOLOGICAL TESTS; RNA, MESSENGER; SWIMMING;

EID: 64049083316     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2008.11.003     Document Type: Article

References (83)

1. 2 inhalation. Eur. J. Pharmacol. 261 (1994) 317-320
2. Barbaccia M.L., Concas A., Serra M., and Biggio G. Stress and neurosteroids in adult and aged rats. Exp. Gerontol. 33 (1998) 697-712
3. Baulieu E.E. Steroid hormones in the brain: several mechanisms?. In: Fuxe K., Gustafsson J.A., and Wetterberg L. (Eds). Steroid Hormone Regulation of the Brain (1981), Pergamon Press, Oxford 3-14
4. Bernardi M., Vergoni A.V., Sandrini M., Tagliavini S., and Bertolini A. Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression. Physiol. Behav. 45 (1989) 1067-1068
5. Biggio G., Concas A., Corda M.G., Giorgi O., Sanna E., and Serra M. GABAergic and dopaminergic transmission in the rat cerebral cortex: effect of stress, anxiolytic and anxiogenic drugs. Pharmacol. Ther. 48 (1990) 121-142
6. A receptor. Brain Res. 561 (1991) 157-161
7. Cooke G.M. Differential effects of trilostane and cyanoketone on the 3β-hydroxysteroid dehydrogenase-isomerase reactions in androgen and 16-androstene biosynthetic pathways in the pig testis. J. Steroid. Biochem. Mol. Biol. 58 (1996) 95-101
8. Crawley J.N., Glowa J.R., Majewska M.D., and Paul S.M. Anxiolytic activity of an endogenous adrenal steroid. Brain Res. 398 (1986) 382-385
9. Dias B.G., Banerjee S.B., Duman R.S., and Vaidya V.A. Differential regulation of brain derived neurotrophic factor transcripts by antidepressant treatments in the adult rat brain. Neuropharmacology 45 (2003) 553-563
10. Dong E., Matsumoto K., Uzunova V., Sugaya I., Takahata H., and Nomura H. Brain 5α-dihydroprogesterone and allopregnanolone synthesis in a mouse model of protracted social isolation. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 2849-2854
11. Epstein R., Erikson L.B., and Reynolds S.R. Reserpine and the chronic stress of reduced barometric pressure in female rats. Observations on body weight, adrenal weight and histology and hematocrit values. Endocrinology 66 (1960) 167-174
12. Eser D., Schüle C., Baghai T.C., Romeo E., and Rupprecht R. Neuroactive steroids in depression and anxiety disorders: clinical studies. Neuroendocrinology 84 (2006) 244-254
13. Flood J.F., Morley J.E., and Roberts E. Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 1567-1571
14. George M.S., Guidotti A., Rubinow D., Pan B., Mikalauskas K., and Post R.M. CSF neuroactive steroids in affective disorders: pregnenolone, progesterone, and DBI. Biol. Psychiatry 35 (1994) 775-780
15. Gibbs T.T., Yagoubi N., Weaver C.E., Park-Chung M., Russek S.J., and Farb D.H. Modulation of ionotropic glutamate receptors by neuroactive steroids. In: Baulieu E.E., Robel P., and Schumacher M. (Eds). Neurosteroids: A New Regulatory Function in the Nervous System (1999), Humana Press, Totowa 167-190
16. Girdler S.S., and Klatzkin R. Neurosteroids in the context of stress: implications for depressive disorders. Pharmacol. Ther. 116 (2007) 125-139
17. Girdler S.S., Straneva P.A., Light K.C., Pedersen C.A., and Morrow A.L. Allopregnanolone levels and reactivity to mental stress in premenstrual dysphoric disorder. Biol. Psychiatry 49 (2001) 788-797
18. Givalois L., Marmigère F., Rage F., Ixart G., Arancibia S., and Tapia-Arancibia L. Immobilization stress rapidly and differentially modulates BDNF and TrkB mRNA expression in the pituitary gland of adult male rats. Neuroendocrinology 74 (2001) 148-159
19. Givalois L., Arancibia S., Alonso G., and Tapia-Arancibia L. Expression of brain-derived neurotrophic factor and its receptors in the median eminence cells with sensitivity to stress. Endocrinology 145 (2004) 4737-4747
20. Givalois L., Naert G., Rage F., Ixart G., Arancibia S., and Tapia-Arancibia L. A single brain-derived neurotrophic factor injection modifies hypothalamo-pituitary-adrenocortical axis activity in adult male rats. Mol. Cell. Neurosci. 27 (2004) 280-295
21. Golubchik P., Lewis M., Maayan R., Sever J., Strous R., and Weizman A. Neurosteroids in child and adolescent psychopathology. Eur. Neuropsychopharmacol. 17 (2007) 157-164
22. Gourley, S.L., Kiraly, D.D., Howell, J.L., Olausson, P., Taylor, J.R., 2008. Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol. Psychiatry. 64, 884-890.
23. Guo A.L., Petraglia F., Criscuolo M., Ficarra G., Nappi R.E., Palumbo M.A., Trentini G.P., Purdy R.H., and Genazzani A.R. Evidence for a role of neurosteroids in modulation of diurnal changes and acute stress-induced corticosterone secretion in rats. Gynecol. Endocrinol. 9 (1995) 1-7
24. Hiwatashi A., Hamamoto I., and Ichikawa Y. Purification and kinetic properties of 3β-hydroxysteroid-dehydrogenase from bovine adrenocortical microsomes. J. Biochem. 98 (1985) 1519-1526
25. Holzbauer M., and Newport H.M. The effect of stress on the concentration of 3β-hydroxypregn-5-en-20-one (pregnenolone) and pregn-4-ene-3,20-dione (progesterone) in the adrenal gland of the rat. J. Physiol. 193 (1967) 131-140
26. Inano H., Hayashiyama J., and Tamaoki B.I. Solubilization of Δ4-3β-hydroxysteroid dehydrogenase with Δ5-Δ4-isomerase and 17β-hydroxysteroid dehydrogenase from rat testicular microsomal fraction by several detergents. J. Steroid. Biochem. 16 (1982) 587-593
27. Iyengar S., Mick S., Dilworth V., Michel J., Rao T.S., Farah J.M., and Wood P.L. Sigma receptors modulate the hypothalamicpituitary-adrenal (HPA) axis centrally: evidence for a functional interaction with NMDA receptors, in vivo. Neuropharmacology 29 (1990) 299-303
28. Karege F., Perret G., Bondolfi G., Schwald M., Bertschy G., and Aubry J.M. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res. 109 (2002) 143-148
29. Khisti R.T., Chopde C.T., and Jain S.P. Antidepressant-like effect of the neurosteroid 3α-hydroxy-5α-pregnan-20-one in mice forced swim test. Pharmacol. Biochem. Behav. 67 (2000) 137-143
30. Kozisek M.E., Middlemas D., and Bylund D.B. Brain-derived neurotrophic factor and its receptor tropomyosin-related kinase B in the mechanism of action of antidepressant therapies. Pharmacol. Ther. 117 (2008) 30-51
31. Liere P., Akwa Y., Weill-Engerer S., Eychenne B., Pianos A., Robel P., Sjövall J., Schumacher M., and Baulieu E.E. Validation of an analytical procedure to measure trace amounts of neurosteroids in brain tissue by gas chromatography-mass spectrometry. J. Chromatogr. B. Biomed. Sci. Appl. 739 (2000) 301-312
32. MacKenzie E.M., Odontiadis J., Le Mellédo J.M., Prior T.I., and Baker G.B. The relevance of neuroactive steroids in schizophrenia, depression, and anxiety disorders. Cell. Mol. Neurobiol. 27 (2007) 541-574
33. A receptor. Mechanism of action and physiological significance. Prog. Neurobiol. 38 (1992) 379-395
34. Majewska M.D., Mienville J.M., and Vicini S. Neurosteroid pregnenolone sulfate antagonizes electrophysiological responses to GABA in neurons. Neurosci. Lett. 90 (1988) 279-284
35. Martin A., Kaufman J., and Charney D. Pharmacotherapy of early-onset depression. Update and new directions. Child Adolesc. Psychiatr. Clin. N. Am. 9 (2000) 135-157
36. Martínez-Mota L., Contreras C.M., and Saavedra M. Progesterone reduces immobility in rats forced to swim. Arch. Med. Res. 30 (1999) 286-289
37. Marx C.E., Shampine L.J., Khisti R.T., Trost W.T., Bradford D.W., Grobin A.C., Massing M.W., Madison R.D., Butterfield M.I., Lieberman J.A., and Morrow A.L. Olanzapine and fluoxetine administration and coadministration increase rat hippocampal pregnenolone, allopregnanolone and peripheral deoxycorticosterone: implications for therapeutic actions. Pharmacol. Biochem. Behav. 84 (2006) 609-617
38. Matsumoto K., Uzunova V., Pinna G., Taki K., Uzunov D.P., and Watanabe H. Permissive role of brain allopregnanolone content in the regulation of pentobarbital-induced righting reflex loss. Neuropharmacology 38 (1999) 955-963
39. 25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 83 (1998) 413-428
40. 1 receptor function: behavioral consequences and therapeutic opportunities. Brain Res. Rev. 37 (2001) 116-132
41. Melchior C.L., and Ritzmann R.F. Dehydroepiandrosterone is an anxiolytic in mice on the plus maze. Pharmacol. Biochem. Behav. 47 (1994) 437-441
42. 3H]norepinephrine release evoked by N-methyl-D-aspartate in the rat hippocampus. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 3774-3778
43. Naert G., Ixart G., Tapia-Arancibia L., and Givalois L. Continuous i.c.v. infusion of brain-derived neurotrophic factor modifies hypothalamic-pituitary-adrenal axis activity, locomotor activity and body temperature rhythms in adult male rats. Neuroscience 139 (2006) 779-789
44. Naert G., Maurice T., Tapia-Arancibia L., and Givalois L. Neuroactive steroids modulate HPA axis activity and cerebral brain-derived neurotrophic factor (BDNF) protein levels in adult male rats. Psychoneuroendocrinology 32 (2007) 1062-1078
45. Patchev V.K., Hassan A.H., Holsboer D.F., and Almeida O.F. The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15 (1996) 533-540
46. Phan V.L., Su T.P., Privat A., and Maurice T. Modulation of steroidal levels by adrenalectomy/castration and inhibition of neurosteroid synthesis enzymes affect sigma1 receptor-mediated behaviour in mice. Eur. J. Neurosci. 11 (1999) 2385-2396
47. Potts G.O., Creange J.E., Hardomg H.R., and Schane H.P. Trilostane, an orally active inhibitor of steroid biosynthesis. Steroids 32 (1978) 257-267
48. Rabe T., Kiesel L., Kellermann J., Weidenhammer K., Runnebaum B., and Potts G.O. Inhibition of human placental progesterone synthesis and aromatase activity by synthetic steroidogenic inhibitors in vitro. Fertil. Steril. 39 (1985) 829-835
49. Rasmusson A.M., Pinna G., Paliwal P., Weisman D., Gottschalk C., Charney D., Krystal J., and Guidotti A. Decreased cerebrospinal fluid allopregnanolone levels in women with posttraumatic stress disorder. Biol. Psychiatry 60 (2006) 704-713
50. Reddy D.S., and Kulkarni S.K. Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Res. 752 (1997) 61-71
51. 1) receptor mediated antidepressant-like effects of neurosteroids in the Porsolt forced swim test. Neuroreport 9 (1998) 3069-3073
52. Robel P., Young J., Corpéchot C., Mayo W., Perché F., Haug M., Simon H., and Baulieu E.E. Biosynthesis and assay of neurosteroids in rats and mice: functional correlates. J. Steroid Biochem. Mol. Biol. 53 (1995) 355-360
53. Robichaud M., and Debonnel G. Modulation of the firing activity of female dorsal raphe nucleus serotonergic neurons by neuroactive steroids. J. Endocrinol. 182 (2004) 11-21
54. Romeo E., Ströhle A., Spalletta G., di Michele F., Hermann B., Holsboer F., Pasini A., and Rupprecht R. Effects of antidepressant treatment on neuroactive steroids in major depression. Am. J. Psychiatry 155 (1998) 910-913
55. Rupprecht R. Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 28 (2003) 139-168
56. Sabeti J., Nelson T.E., Purdy R.H., and Gruol D.L. Steroid pregnenolone sulfate enhances NMDA-receptor-independent long-term potentiation at hippocampal CA1 synapses: role for L-type calcium channels and sigma-receptors. Hippocampus 17 (2007) 349-369
57. Schmidt P.J., Daly R.C., Bloch M., Smith M.J., Danaceau M.A., St Clair L.S., Murphy J.H., Haq N., and Rubinow D.R. Dehydroepiandrosterone monotherapy in midlife-onset major and minor depression. Arch. Gen. Psychiatry 62 (2005) 154-162
58. Schulte D.M., Shapiro I., Reincke M., and Beuschlein F. Expression and spatio-temporal distribution of differentiation and proliferation markers during mouse adrenal development. Gene Expr. Patterns 7 (2007) 72-81
59. Serra M., Pisu G.M., Muggironi M., Parodo V., Papi G., Sari R., Dazzi L., Spiga F., Purdy R.H., and Biggio G. Opposite effects of short- versus long-term administration of fluoxetine on the concentrations of neuroactive steroids in rat plasma and brain. Psychopharmacology 158 (2001) 48-54
60. Shirayama Y., Chen A.C.H., Nakagawa S., Russell D.S., and Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22 (2002) 3251-3261
61. Siuciak J.A., Lewis D.R., Wiegand S.J., and Lindsay R.M. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol. Biochem. Behav. 56 (1997) 131-137
62. A-antagonistic neurosteroids in patients with combat-related post-traumatic stress disorder. Psychol. Med. 30 (2000) 1227-1231
63. Strekalova T., Spanagel R., Bartsch D., Henn F.A., and Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29 (2004) 2007-2017
64. Ströhle A., Romeo E., Hermann B., Pasini A., Spalletta G., di Michele F., Holsboer F., and Rupprecht R. Concentrations of 3α-reduced neuroactive steroids and their precursors in plasma of patients with major depression and after clinical recovery. Biol. Psychiatry 45 (1999) 274-277
65. Ströhle A., Pasini A., Romeo E., Hermann B., Spalletta G., and di Michele F. Fluoxetine decreases concentrations of 3α,5α-tetrahydrodeoxycorticosterone (THDOC) in major depression. J. Psychiatr. Res. 34 (2000) 183-186
66. Su T.P., London E.D., and Jaffe J.H. Steroid binding at σ receptors suggests a link between endocrine, nervous, and immune systems. Science 240 (1988) 219-221
67. Takahashi M., Luu-The V., and Labrie F. Inhibitory effect of synthetic progestins, 4-MA and cyanoketone on human placental 3β-hydroxysteroid dehydrogenase/5-4-ene-isomerase activity. J. Steroid Biochem. Mol. Biol. 37 (1990) 231-236
68. Tapia-Arancibia L., Rage F., Givalois L., and Arancibia S. Physiology of BDNF: focus on hypothalamic function. Front. Neuroendocrinol. 25 (2004) 77-107
69. 1-receptor agonists and neuroactive steroids in mice submitted to the forced swimming test. J. Pharmacol. Exp. Ther. 298 (2001) 1269-1279
70. Uzunov D.P., Cooper T.B., Costa E., and Guidotti A. Fluoxetine-elicited changes in brain neurosteroid content measured by negative ion mass fragmentography. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 12599-12604
71. Uzunova V., Sheline Y., Davis J.M., Rasmusson A., Uzunov D.P., Costa E., and Guidotti A. Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3239-3244
72. Uzunova V., Ceci M., Kohler C., Uzunov D.P., and Wrynn A.S. Region-specific dysregulation of allopregnanolone brain content in the olfactory bulbectomized rat model of depression. Brain Res. 976 (2003) 1-8
73. Uzunova V., Wrynn A.S., Kinnunen A., Ceci M., Kohler C., and Uzunov D.P. Chronic antidepressants reverse cerebrocortical allopregnanolone decline in the olfactory-bulbectomized rat. Eur. J. Pharmacol. 486 (2004) 31-34
74. Vallée M., Rivera J.D., Koob G.F., Purdy R.H., and Fitzgerald R.L. Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Anal. Biochem. 287 (2000) 153-166
75. Whitnall M.H. Regulation of the hypothalamic corticotropin releasing hormone neurosecretory system. Prog. Neurobiol. 40 (1993) 573-629
76. Wieland S., Lan N.C., Mirasedeghi S., and Gee K.W. Anxiolytic activity of the progesterone metabolite 5α-pregnan-3α-ol-20-one. Brain Res. 565 (1991) 263-268
77. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52 (2005) 90-110
78. Wolkowitz O.M., Reus V.I., Roberts E., Manfredi F., Chan T., Ormiston S., Johnson R., Canick J., Brizendine L., and Weingartner H. Antidepressant and cognition-enhancing effects of DHEA in major depression. Ann. N. Y. Acad. Sci. 774 (1995) 337-339
79. Wolkowitz O.M., Reus V.I., Roberts E., Manfredi F., Chan T., Raum W.J., Ormiston S., Johnson R., Canick J., Brizendine L., and Weingartner H. Dehydroepiandrosterone (DHEA) treatment of depression. Biol. Psychiatry 41 (1997) 311-318
80. Wolkowitz O.M., Reus V.I., Chan T., Manfredi F., Raum W., Johnson R., and Canick J. Antiglucocorticoid treatment of depression: double-blind ketoconazole. Biol. Psychiatry 45 (1999) 1070-1074
81. Wu F.S., Gibbs T.T., and Farb D.H. Pregnenolone sulfate: A positive allosteric modulator at the N-methyl-D-aspartate receptor. Mol. Pharmacol. 40 (1991) 333-336
82. Young J., Corpéchot C., Perché F., Haug M., Baulieu E.E., and Robel P. Neurosteroids: pharmacological effects of a 3β-hydroxy-steroid dehydrogenase inhibitor. Endocrine 2 (1994) 505-509
83. Young J., Corpéchot C., Perché F., Eychenne B., Haug M., Baulieu E.E., and Robel P. Neurosteroids in the mouse brain: behavioral and pharmacological effects of a 3β-hydroxysteroid dehydrogenase inhibitor. Steroids 61 (1996) 144-149