Stress-Induced Deoxycorticosterone-Derived Neurosteroids Modulate GABA A Receptor Function and Seizure Susceptibility

Journal of Neuroscience

Volumn 22, Issue 9, 2002, Pages 3795-3805

  Reddy, Doodipala S ^a,b   Rogawski, Michael A ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

5 ,3 tetrahydrodeoxycorticosterone (3 ,21 dihydroxy 5 pregnan 20 one); 5 dihydrodeoxycorticosterone; Deoxycorticosterone; Finasteride; Indomethacin; Kindling; Neurosteroid; Pentylenetetrazol; Seizure; Stress

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 ETHYL 6,7 DIMETHOXY BETA CARBOLINE 3 CARBOXYLIC ACID METHYL ESTER; 5ALPHA DIHYDRODEOXYCORTICOSTERONE; ALLOTETRAHYDRODEOXYCORTICOSTERONE; CORTICOSTERONE DERIVATIVE; DEOXYCORTICOSTERONE; FINASTERIDE; INDOMETACIN; NEUROSTEROID; PENTETRAZOLE; PICROTOXIN; STEROID 5ALPHA REDUCTASE INHIBITOR; UNCLASSIFIED DRUG; 5 DIHYDRODEOXYCORTICOSTERONE; 5-DIHYDRODEOXYCORTICOSTERONE; CONVULSANT AGENT; CORTICOSTERONE; DRUG DERIVATIVE; ENZYME INHIBITOR; NONSTEROID ANTIINFLAMMATORY AGENT; STEROID; STEROID 5ALPHA REDUCTASE; TETRAHYDRODEOXYCORTICOSTERONE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICONVULSANT ACTIVITY; ARTICLE; CHLORIDE CURRENT; CONTROLLED STUDY; CORTICOSTEROID BLOOD LEVEL; FORCED SWIMMING TEST; KINDLING; MALE; NONHUMAN; PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SEIZURE SUSCEPTIBILITY; SEIZURE THRESHOLD; ADRENALECTOMY; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE PREDISPOSITION; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; EXERCISE TEST; METABOLISM; MOTOR ACTIVITY; MOUSE; PATHOPHYSIOLOGY; SEIZURE; SPRAGUE DAWLEY RAT; STRESS;

ADRENALECTOMY; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CONVULSANTS; CORTICOSTERONE; DESOXYCORTICOSTERONE; DISEASE SUSCEPTIBILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ANTAGONISM; DRUG RESISTANCE; ENZYME INHIBITORS; EXERCISE TEST; FINASTERIDE; INDOMETHACIN; KINDLING, NEUROLOGIC; MALE; MICE; MOTOR ACTIVITY; PENTYLENETETRAZOLE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SEIZURES; STEROIDS; STRESS; TESTOSTERONE 5-ALPHA-REDUCTASE;

EID: 0036582315     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-09-03795.2002     Document Type: Article

References (69)

1. Abel EL, Berman RF (1993) Effects of water immersion stress on convulsions induced by pentylenetetrazol. Pharmacol Biochem Behav 45:823-825.
2. Albertson TE, Peterson SL, Stark LG (1980) Anticonvulsant drugs and their antagonism of kindled amygdaloid seizures in rats. Neuropharmacology 19:643-652.
3. Azzolina B, Ellsworth K, Andersson S, Geissler W, Bull HG, Harris GS (1997) Inhibition of rat 5α-reductases by finasteride: evidence for isozyme differences in the mechanism of inhibition. J Steroid Biochem Mol Biol 61:55-64.
4. A receptor function after acute stress. Neuroendocrinology 63:166-172.
5. Barbaccia 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.
6. Beyer C, Gonzalez-Flores O, Ramirez-Orduna JM, Gonzalez-Mariscal G (1999) Indomethacin inhibits lordosis induced by ring A-reduced progestins: possible role of 3α-oxidoreduction in progestin-facilitated lordosis. Horm Behav 35:1-8.
7. A receptor. Brain Res 561:157-161.
8. A receptor. J Pharmacol Exp Ther 280:1284-1295.
9. Charbonneau A, The VL (2001) Genomic organization of a human 5β-reductase and its pseudogene and substrate selectivity of the expressed enzyme. Biochim Biophys Acta 1517:228-235.
10. Conforti N, Feldman S (1975) Effect of cortisol on the excitability of limbic structures of the brain in freely moving rats. J Neurol Sci 26:29-38.
11. Coughenour AG, McLean JR, Parker RB (1977) A new device for the rapid measurement of impaired motor function in mice. Pharmacol Biochem Behav 6:351-353.
12. Craig CR (1966) Anticonvulsant activity of steroids: separability of anticonvulsant from hormonal effects. J Pharmacol Exp Ther 153:337-343.
13. Crawley JN, Glowa JR, Majewska MD, Paul SM (1986) Anxiolytic activity of an endogenous adrenal steroid. Brain Res 398:382-385.
14. Donevan SD, Jones SM, Rogawski MA (1992) Arcaine blocks N-methyl-D-aspartate receptor responses by an open channel mechanism: whole-cell and single-channel recording studies in cultured hippocampal neurons. Mol Pharmacol 41:727-735.
15. Feldman RG, Paul NL (1976) Identity of emotional triggers in epilepsy. J Nerv Ment Dis 162:345-353.
16. Ferngren H (1969) High frequency electro-shock seizures and their antagonism in developing mice. III. Effects of cortisol, corticosterone, deoxycorticosterone, dexamethasone and a synthetic corticotropine. Acta Pharm Suec 6:339-348.
17. Frucht MM, Quigg M, Schwaner C, Fountain NB (2000) Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 41:1534-1539.
18. Gallo MA, Smith SS (1993) Progesterone withdrawal decreases latency to and increases duration of electrified prod burial: a possible rat model of PMS anxiety. Pharmacol Biochem Behav 46:897-904.
19. Gasior M, Ungard JT, Beekman M, Carter RB, Witkin JM (2000) Acute and chronic effects of the synthetic neuroactive steroid, ganaxolone, against the convulsive and lethal effects of pentylenetetrazol in seizure-kindled mice: comparison with diazepam and valproate. Neuropharmacology 39:1184-1196.
20. Goldberg ME, Salama AI (1969) Effect of drum stress on maximal electroconvulsive seizure latency in mice. Int J Neuropharmacol 8:161-167.
21. Harrison NL, Majewska MD, Harrington JW, Barker JL (1987) Structure-activity relationships for steroid interactions with the γ-aminobutyric acid-A receptor complex. J Pharmacol Exp Ther 241:346-353.
22. Heuser E, Eidelberg E (1961) Steroid-induced convulsions in experimental animals. Endocrinology 69:915-924.
23. Kater CE, Biglieri EG, Brust N, Chang B, Hirai J, Irony I (1989) Stimulation and suppression of the mineralocorticoid hormones in normal subjects and adrenocortical disorder. Endocr Rev 10:149-164.
24. Kawahara FS, Berman ML, Green OC (1975) Conversion of progesterone-1,2-3-H to 5β-pregnane-3,20-dione by brain tissue. Steroids 25:459-463.
25. Kokate TG, Svensson BE, Rogawski MA (1994) Anticonvulsant activity of neurosteroids: correlation with γ-aminobutyric acid-evoked chloride current potentiation. J Pharmacol Exp Ther 270:1223-1229.
26. Kokate TG, Cohen AL, Karp E, Rogawski MA (1996) Neuroactive steroids protect against pilocarpine- and kainic acid-induced limbic seizures and status epilepticus in mice. Neuropharmacology 35:1049-1056.
27. Kokate TG, Banks MK, Magee T, Yamaguchi S, Rogawski MA (1999) Finasteride, a 5α-reductase inhibitor, blocks the anticonvulsant activity of progesterone in mice. J Pharmacol Exp Ther 288:679-684.
28. A receptor complex: electrophysiological studies. Ciba Found Symp 153:56-71.
29. A receptor function. Trends Pharmacol Sci 16:295-303.
30. Li X, Bertics PJ, Karavolas HJ (1997) Regional distribution of cytosolic and particulate 5α-dihydroprogesterone 3α-hydroxysteroid oxidoreductases in female rat brain. J Steroid Biochem Mol Biol 60:311-318.
31. Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232:1004-1007.
32. Mensah-Nyagan AG, Do-Rego JL, Beaujean D, Luu-The V, Pelletier G, Vaudry H (1999) Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system. Pharmacol Rev 51:63-81.
33. Minter RE (1979) Can emotions precipitate seizures: a review of the question. J Fam Pract 8:55-59.
34. Morimoto K, Sanei T, Sato K (1993) Comparative study of the anticonvulsant effect of γ-aminobutyric acid agonists in the feline kindling model of epilepsy. Epilepsia 34:1123-1129,
35. Morimoto K, Sato H, Yamamoto Y, Watanabe T, Suwaki H (1997) Antiepileptic effects of tiagabine, a selective GABA uptake inhibitor, in the rat kindling model of temporal lobe epilepsy. Epilepsia 38:966-974.
36. Normington K, Russell DW (1992) Tissue distribution and kinetic characteristics of rat steroid 5α-reductase isozymes: evidence for distinct physiological functions. J Biol Chem 267:19548-19554.
37. A receptor function through distinct sites. Brain Res 830:72-87.
38. Penning TM, Talalay P (1983) Inhibition of a major NAD(P)-linked oxidoreductase from rat liver cytosol by steroidal and nonsteroidal anti-inflammatory agents and by prostaglandins. Proc Natl Acad Sci USA 80:4504-4508.
39. Penning TM, Sharp RB, Krieger NR (1985) Purification and properties of 3α-hydroxysteroid dehydrogenase from rat brain cytosol. Inhibition by nonsteroidal anti-inflammatory drugs and progestins. J Biol Chem 260:15266-15272.
40. Peričić D, Svob D, Jazvinšćak M, Mirković K (2000) Anticonvulsive effect of swim stress in mice. Pharmacol Biochem Behav 66:879-886.
41. Peričić D, Jazvinšćak M, Svob D, Mirković K (2001) Swim stress alters the behavioural response of mice to GABA-related and some GABA-unrelated convulsants. Epilepsy Res 43:145-152.
42. Poletti A, Celotti F, Maggi R, Melcangi RC, Martini L, Negri-Cesi P (1999) Aspects of hormonal steroid metabolism in the nervous system. In: Contemporary endocrinology: neurosteroids: a new regulatory function in the nervous system (Baulieu E-E, Robel P, Schumacher M, eds), pp 97-123. Totowa, NJ: Humana.
43. Purdy RH, Morrow AL, Blinn JR, Paul SM (1990) Synthesis, metabolism, and pharmacological activity of 3α-hydroxy steroids which potentiate GABA-receptor-mediated chloride ion uptake in rat cerebral cortical synaptoneurosomes. J Med Chem 33:1572-1581.
44. Purdy RH, Morrow AL, Moore Jr PH, Paul SM (1991) Stress-induced elevations of γ-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci USA 88:4553-4557.
45. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
46. Reddy DS, Kulkarni SK (2000) Development of neurosteroid-based novel psychotropic drugs. Prog Med Chem 37:135-175.
47. Reddy DS, Rogawski MA (2000) Enhanced anticonvulsant activity of ganaxolone after neurosteroid withdrawal in a rat model of catamenial epilepsy. J Pharmacol Exp Ther 294:909-915.
48. Reddy DS, Rogawski MA (2001) Enhanced anticonvulsant activity of neuroactive steroids in a rat model of catamenial epilepsy. Epilepsia 42:337-344.
49. Reddy DS, Kim H-Y, Rogawski MA (2001) Neurosteroid withdrawal model of perimenstrual catamenial epilepsy. Epilepsia 42:328-336.
50. Roberts AJ, Keith LD (1994) Mineralocorticoid receptors mediate the enhancing effects of corticosterone on convulsion susceptibility in mice. J Pharmacol Exp Ther 270:505-511.
51. Rogawski MA, Porter RJ (1990) Antiepileptic drugs: pharmacological mechanisms and clinical efficacy with consideration of promising developmental stage compounds. Pharmacol Rev 42:223-286.
52. Rogawski MA, Kurzman PS, Yamaguchi S, Li H (2001) Role of AMPA and GluR5 kainate receptors in the development and expression of amygdala kindling in the mouse. Neuropharmacology 40:28-35.
53. Russell DW, Wilson JD (1994) Steroid 5α-reductase: two genes/two enzymes. Annu Rev Biochem 63:25-61.
54. Segal M (1983) Rat hippocampal neurons in culture: response to electrical and chemical stimuli. J Neurophysiol 50:1249-1264.
55. Selye H (1942) The antagonism between anesthetic steroid hormones and pentamethylenetetrazol (metrazol). J Lab Clin Med 27:1051-1053.
56. A receptor function in rat brain. J Neurochem 75:732-740.
57. A receptor α4 subunit in association with increased anxiety. J Neurosci 18:5275-5284.
58. Smithgall TE, Penning TM (1985) Indomethacin-sensitive 3-hydroxy-steroid dehydrogenase in rat tissues. Biochem Pharmacol 34:831-835.
59. 3H]flunitrazepam cortical binding following stressful manipulations in rats. Brain Res 189:505-517.
60. Stoffel-Wagner B, Beyenburg S, Watzka MS, Blumcke I, Bauer J, Schramm J, Bidlingmaier F, Elger CE (2000) Expression of 5α-reductase and 3α-hydroxisteroid oxidoreductase in the hippocampus of patients with chronic temporal lobe epilepsy. Epilepsia 41:140-147.
61. Tan SY, Mulrow PJ (1975) The contribution of the zona fasciculata and glomerulosa to plasma 11-deoxycorticosterone levels in man. J Clin Endocrinol Metab 41:126-130.
62. Temkin NR, Davis GR (1984) Stress as a risk factor for seizures among adults with epilepsy. Epilepsia 25:450-456.
63. Thigpen AE, Russell DW (1992) Four-amino acid segment in steroid 5α-reductase 1 confers sensitivity to finasteride, a competitive inhibitor. J Biol Chem 267:8577-8583.
64. Vallee M, Rivera JD, Koob GF, Purdy RH, Fitzgerald RL (2000) Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Anal Biochem 287:153-166.
65. von Steiger M, Reichstein T (1937) Desoxy-cortico-steron (21-oxyprogesteron) aus Δ5-3-oxy-atio-cholensaure. Helv Chim Acta 20:1164-1179.
66. - currents in cultured rat hypothalamic neurons. Br J Pharmacol 127:863-868.
67. White HS, Woodhead JH, Franklin MR, Swinyard EA, Wolf HA (1995) General principles: experimental selection, quantification, and evaluation of antiepileptic drugs. In: Antiepileptic drugs, Ed 4 (Levy RH, Mattson RH, Meldrum BS, eds), pp 99-110. New York: Raven.
68. Woodbury DM, Davenport VD (1949) Brain and plasma cations and experimental seizures in normal and desoxycorticosterone-treated rats. Am J Physiol 157:234-240.
69. Yokoi H, Tsuruo Y, Miyamoto T, Ishimura K (1998) Steroid 5α-reductase type 1 immunolocalized in the adrenal gland of normal, gonadectomized, and sex hormone-supplemented rats. Histochem Cell Biol 109:127-134.