Neuroactive steroid 3α-hydroxy-5α-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol

Journal of Neuroscience

Volumn 20, Issue 5, 2000, Pages 1982-1989

  VanDoren, Margaret J ^a,b   Matthews, Douglas B ^a,e   Janis, Gregory C ^a,c   Grobin, A Chistina ^a   Devaud, Leslie L ^a,d   Morrow, A Leslie ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^d IDAHO STATE UNIVERSITY   (United States)

^e University of Memphis   (United States)

Author keywords

3 hydroxy 5 pregnan 20 one; Allopregnanolone; Ethanol; Finasteride; Neuroactive steroids; Nongenomic steroid actions

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ALCOHOL; CORTICOSTERONE; FINASTERIDE; INDOMETACIN; NEUROSTEROID; PROGESTERONE; STEROID; STEROID 5ALPHA REDUCTASE INHIBITOR; TRILOSTANE; 4 AMINOBUTYRIC ACID A RECEPTOR; ANDROSTANOLONE; BICUCULLINE; CENTRAL DEPRESSANT AGENT; CONVULSANT AGENT; DRUG DERIVATIVE; ELTANOLONE; ENZYME INHIBITOR; NEUROPROTECTIVE AGENT; PROSTAGLANDIN SYNTHASE INHIBITOR;

ALCOHOL CONSUMPTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG EFFECT; HORMONAL REGULATION; HORMONE ACTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RIGHTING REFLEX; SEIZURE THRESHOLD; ANIMAL; BRAIN LEVEL; CHEMICALLY INDUCED DISORDER; ELECTROPHYSIOLOGY; EPILEPSY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BEHAVIOR, ANIMAL; BICUCULLINE; BRAIN CHEMISTRY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBRAL CORTEX; CONVULSANTS; CYCLOOXYGENASE INHIBITORS; DIHYDROTESTOSTERONE; ELECTROPHYSIOLOGY; ENZYME INHIBITORS; EPILEPSY; ETHANOL; FINASTERIDE; INDOMETHACIN; MALE; NEUROPROTECTIVE AGENTS; PREGNANOLONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

EID: 0034144699     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-05-01982.2000     Document Type: Article

References (58)

1. A receptor function after acute stress. Neuroendocrinology 63:166-172.
2. Barhaccia ML, Roscetti G, Trabucchi M, Purdy RH, Mostallino MC, Concas A, Biggio G (1997) The effects of inhibitors of GABAergic transmission and stress on brain and plasma allopregnanolone concentrations. Br J Pharmacol 120:1582-1588.
3. Bowen CA, Purdy RH, Grant KA (1999) An investigation of endogenous neuroactive steroid-induced modulation of ethanol's discriminative stimulus effects. Behav Pharmacol 10:297-311.
4. Bramson HN, Hermann D, Batchelor KW, Lee FW, James MK, Frye SV (1997) Unique preclinical characteristics of GC745, a potent dual inhibitor of 5AR. J Pharmacol Exp Ther 282:1496-1502.
5. Cascio C, Prasad VVK, Lin YY, Lieberman S, Papadopoulos V (1998) Detection of P450c17-independent pathways for dehydroepiandrosterone (DHEA) biosynthesis in brain glial tumor cells. Proc Natl Acad Sci USA 95:2862-2867.
6. Concas A, Mostallino MC, Porcu P, Follesa P, Barbaccia ML, Trabucchi M, Purdy RH, Grisenti P, Biggio G (1998) Role of brain allopregnanolone in the plasticity of gamma-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci USA 95:13284-13289.
7. A currents insensitive to benzodiazepine modulation in rat CA1 hippocampus. J Neurophysiol 74:464-469.
8. Crews F, Morrow AL, Criswell H, Breese G (1996) Effects of ethanol on ion channels. In: International review of neurobiology, Vol 39 (Bradley RJ, Harris RA, eds), pp 283-367. New York: Academic.
9. A receptor subunit mRNAs in rat cerebral cortex: competitive, quantitative reverse transcriptase-polymerase chain reaction analysis. Mol Pharmacol 48:861-868.
10. A receptors to neuroactive steroids in rats during ethanol withdrawal. J Pharmacol Exp Ther 278:510-517.
11. Devaud LL, Fritschy J-M, Sieghart W, Morrow AL (1997) Bidirectional alterations of GABAA receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J Neurochem 69:126-130.
12. Finn DA, Gee KW (1993) The influence of estrus cycle on neurosteroid potency at the gamma-aminobutyric acidA receptor complex. J Pharmacol Exp Ther 265:1374-1379.
13. A-activated currents in adult medial septum/diagonal band neurons. Brain Res 635:283-292.
14. Givens BS, Breese GR (1990) Site-specific enhancement of γ-aminobutyric acid-mediated inhibition of neural activity by ethanol in the rat medial septum. J Pharmacol Exp Ther 254:528-538.
15. Glowa JR, Crawley J, Suzdak PD, Paul SM (1988) Ethanol and the GABA receptor complex: studies with the partial inverse benzodiazepine receptor agonist Ro 15-4513. Pharmacol Biochem Behav 31:767-772.
16. Griffin LD, Mellon SH (1999) Selective serotonin reuptake inhibitors directly alter activity of neurosteroidogenic enzymes. Proc Natl Acad Sci USA 965:13512-13517.
17. Grobin AC, Matthews DB, Devaud LL, Morrow AL (1998) The role of GABAA receptors in the acute and chronic effects of ethanol. Psychopharmacology 139:2-19.
18. Harrison NL, Majewska MD, Harrington JW, Barker JL (1987) Structure-activity relationships for steroid interaction with the gamma-aminobutyric acid-A receptor complex. J Pharmacol Exp Ther 241:346-353.
19. Ichikawa S, Sawada T, Nakamura Y, Morioka H (1974) Ovarian secretion of pregnane compounds during the estrus cycle and pregnancy in rats. Endocrinology 94:1615-1620.
20. Janak PH, Redfern JEM, Samson HH (1998) The reinforcing effects of ethanol are altered by the endogenous neurosteroid, allopregnanolone. Alcohol Clin Exp Res 22:1106-1112.
21. Janis GC, Devaud LL, Mitsuyama H, Morrow AL (1998) Effects of chronic ethanol consumption and withdrawal on the neuroactive steroid 3α-hydroxy-5α-pregnan-20-one in male and female rats. Alcohol Clin Exp Res 22:2055-2061.
22. Kokate TG, Banks MK, MagooT, Yamaguchi S-I, Rogawski MA (1999) Finasteride, a 5α-reductase inhibitor, blocks the anticonvulsant activity of progesterone in mice. J Pharmacol Exp Ther 288:679-684.
23. Korneyev A, Guidotti A, Costa E (1993a) Regional and interspecies differences in brain progesterone metabolism. J Neurochem 61:2041-2047.
24. Korneyev AY, Costa E, Guidotti A (1993b) During anesthetic-induced activation of hypothalamic pituitary adrenal axis, blood borne steroids fail to contribute to the anesthetic effect. Neuroendocrinology 57:559-565.
25. Lephart ED, Ladle DR, Jacobson NA, Rhees RW (1996) Inhibition of brain 5α-reductase in pregnant rats: Effects on enzymatic and behavioral activity. Brain Res 739:356-360.
26. Lieberman S, Prasad VVK (1990) Heterodox notions of pathways of steroidogenesis. Endocr Rev 11:469-493.
27. Liu Y, Deitrich RA (1998) Role of GABA in the actions of ethanol in rats selectively bred for ethanol sensitivity. Pharmacol Biochem Behav 60:793-801.
28. Mancillas JR, Siggins JR, Bloom FE (1986) Systemic ethanol: enhancement of responses to acetylcholine and somatostatin in hippocampus. Science 231:161-163.
29. Marszalec W, Aistrup GL, Narahashi T (1998) Ethanol modulation of excitatory and inhibitory synaptic interactions in cultured cortical neurons. Alcohol Clin Exp Res 22:1516-1524.
30. Martini L, Celotti F, Melcangi RC (1996) Testosterone and progesterone metabolism in the central nervous system: cellular localization and mechanism of control of the enzymes involved. Cell Mol Biol 16:271-282.
31. Martz A, Dietrich RA, Harris RA (1983) Behavioral evidence for the involvement of γ-aminobutyric acid in the actions of ethanol. Eur J Pharmacol 89:53-62.
32. Matsumoto K, Uzunova V, Pinna G, Taki K, Uzunov DP, Watanabe H, Mienville JM, Guidotti A, Costa E (1999) Permissive role of brain allopregnanolone content in the regulation of pentobarbital-induced righting reflex loss. Neuropharmacology 38:955-963.
33. A receptor gene expression by ethanol in the rat hippocampus vs. cerebral cortex. J Neurochem 70:1160-1166.
34. A receptor function and gene expression in the central nervous system. In: International review of neurobiology, Vol 38 (Bradley RJ, Harris RA, cds), pp 1-41. San Diego: Academic.
35. Morrow AL, Suzdak PD, Paul SM (1987) Steroid hormone metabolites potentiate GABA receptor-mediated chloride ion flux with nanomolar potency. Eur J Pharmacol 142:483-485.
36. Morrow AL, VanDoren MJ, Devaud LL (1998) Effects of progesterone or neuroactive steroid? Nature 395:652-653.
37. Nutt DJ, Lister RG (1989) Antagonizing the anticonvulsant effect of ethanol using drugs acting at the benzodiazepine/GABA receptor complex. Pharmacol Biochem Behav 31:751-755.
38. Paul SM, Purdy RH (1992) Neuroactive steroids. FASEB J 6:2311-2322.
39. Penning TM, Sharp RB, Kriegers NR (1985) Purification and properties of 3α-hydroxysteroid dehydrogenase from rat brain cytosol. J Biol Chem 260:15266-15282.
40. Potts GO, Creange JW, Harding HR, Schane HP (1978) Trilostane, an orally active inhibitor of steroid biosynthesis. Steroids 32:257-267.
41. Prasad VVK, Vegesna SR, Welch M, Lieberman S (1994) Precursors of the neurosteroids. Proc Natl Acad Sci USA 91:3220-3223.
42. Purdy RH, Morrow AL, Moore Jr PH, Paul SM (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.
43. Rastogi SK, Thyagarajan R, Clothier J, Ticku MK (1986) Effect of chronic treatment of ethanol on henzodiazepine and picrotoxin sites on the GABA receptor complex in regions of the brain of the rat. Neuropharmacology 25:1179-1184.
44. Rivier C, Bruhn T, Vale W (1984) Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of corticotropin-releasing factor (CRF). J Pharmacol Exp Ther 229:127-131.
45. Rohel P, Baulieu EE (1995) Neurosteroids: biosynthesis and function. Crit Rev Neurobiol 9:383-395.
46. Roselli CE, Snipes CA (1984) Progesterone 5α-reductase in mouse brain. Brain Res 305:197-202.
47. Rupprecht R, Holsboer F (1999) Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 22:410-416.
48. A receptor interactions: A comparison between cell lines and cerebellar Purkinje cells. J Pharmacol Exp Ther 284:768-776.
49. Schuckit MA, Smith TL (1996) An 8-year follow-up of 450 sons of alcoholic and control subjects. Arch Gen Psychiatry 53:202-210.
50. 36Cl uptake in rat brain synapto-neurosomes: evidence for rapid desensitization of the GABA receptor-coupled chloride ion channel. Mol Pharmacol 30:419-426.
51. Simson PE, Criswell HE, Breese GR (1991) Ethanol potentiates γ-aminobutyric acid-mediated inhibition in the inferior colliculus: evidence for local ethanol/γ-aminobutyric acid interactions. J Pharmacol Exp Ther 259:1288-1293.
52. A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392:926-930.
53. A receptor α4 subunit in association with increased anxiety. J Neurosci 18:5275-5284.
54. Steiner JF (1996) Clinical pharmacokinetics and pharmacodynamics of finasteride. Clin Pharmacokinet 30:16-27.
55. Suzdak PD, Glowa JR, Crawley JN, Schwartz RD, Skolnick P, Paul SM (1986a) A selective imidazobenzodiazepine antagonist of ethanol in the rat. Science 234:1243-1247.
56. Suzdak PD, Schwartz RD, Skolnick P, Paul SM (1986b) Ethanol stimulates γ-aminobutyric acid receptor-mediated chloride transport in rat brain synaptoneurosomes. Proc Natl Acad Sci USA 83:4071-4075.
57. Uzunov DP. Cooper TB, Costa E, Guidotti A (1996) Fluoxetine-elicited changes in brain neurosteroid content measured by negative ion mass fragmentography. Proc Natl Acad Sci USA 93:12599-12604.
58. Uzunova V, Sheline Y, Davis JM, Rasmusson A, Uzunov DP, Costa E, Guidotti A (1998) 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 95:3239-3244.