Development and persistence of limbic epileptogenesis are impaired in mice lacking progesterone receptors

Journal of Neuroscience

Volumn 31, Issue 2, 2011, Pages 650-658

  Reddy, Doodipala Samba ^a   Mohan, Ashwin ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MIFEPRISTONE; NEUROSTEROID; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DRUG ACTIVITY; EPILEPTOGENESIS; FEMALE; HIPPOCAMPUS; LIMBIC SYSTEM; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE;

ANIMALS; ANTICONVULSANTS; DISEASE SUSCEPTIBILITY; EPILEPSY; FEMALE; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; KINDLING, NEUROLOGIC; LIMBIC SYSTEM; MICE; MICE, KNOCKOUT; MIFEPRISTONE; NEUROSECRETORY SYSTEMS; NEUROTRANSMITTER AGENTS; OLIGONUCLEOTIDES, ANTISENSE; PROGESTERONE; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION;

EID: 78651512827     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4488-10.2011     Document Type: Article

References (56)

1. Albertson TE, Joy RM, Stark LG (1984) A pharmacological study in the kindling model of epilepsy. Neuropharmacology 23:1117-1123.
2. Alves SE, McEwen BS, Hayashi S, Korach KS, Pfaff DW, Ogawa S (2000) Estrogen-regulated progestin receptors are found in the midbrain raphe but not hippocampus of estrogen receptor alpha (ER-α) gene-disrupted mice. J Comp Neurol 427:185-195.
3. Auger CJ, De Vries GJ (2002) Progestin receptor immunoreactivity within steroid-responsive vasopressin-immunoreactive cells in the male and female rat brain. J Neuroendocrinol 14:561-567.
4. Biagini G, Baldelli E, Longo D, Pradelli L, Zini I, Rogawski MA, Avoli M (2006) Endogenous neurosteroids modulate epileptogenesis in a model of temporal lobe epilepsy. Exp Neurol 201:519-524. (Pubitemid 44344227)
5. Borowicz KK, Luszczki J, Matuszek M, Kleinrok Z, Czuczwar SJ (2002) Effects of tamoxifen, mifepristone and cyproterone on the electroconvulsive threshold and pentetrazole-induced convulsions in mice. Pol J Pharmacol 54:103-109.
6. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, Morgan TE, Pike CJ, Mack WJ, Stanczyk FZ, Nilsen J (2008) Progesterone receptors: Form and function in brain. Front Neuroendocrinol 29:313-339.
7. Chappell PE, Lydon JP, Conneely OM, O'Malley BW, Levine JE (1997) Endocrine defects in mice carrying a null mutation for the progesterone receptor gene. Endocrinology 138:4147-4152.
8. Chappell PE, Schneider JS, Kim P, Xu M, Lydon JP, O'Malley BW, Levine JE (1999) Absence of gonadotropin surges and gonadotropin-releasing hormone self-priming in ovariectomized (OVX), estrogen (E2)-treated, progesterone receptor knockout (PRKO) mice. Endocrinology 140:3653-3658.
9. Conneely OM, Mulac-Jericevic B, DeMayo F, Lydon JP, O'Malley BW (2002) Reproductive functions of progesterone receptors. Recent Prog Horm Res 57:339-355.
10. Dennison Z, Teskey GC, Cain DP (1995) Persistence of kindling: Effect of partial kindling, retention interval, kindling site, and stimulation parameters. Epilepsy Res 21:171-182.
11. Edwards HE, Epps T, Carlen PL, J MacLusky N (2000) Progestin receptors mediate progesterone suppression of epileptiform activity in tetanized hippocampal slices in vitro. Neuroscience 101:895-906.
12. Franklin KBJ, PaxinosG (1997) The mouse brain in stereotaxic coordinates. San Diego: Academic.
13. Gangisetty O, Reddy DS (2010) Neurosteroid withdrawal regulates GABA-A receptor α4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway. Neuroscience 170:865-880.
14. Goddard GV, McIntyre DC, Leech CK (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295-330.
15. Gowers WR (1881) Epilepsy and other chronic convulsive diseases. London: Churchill.
16. He XP, Kotloski R, Nef S, Luikart BW, Parada LF, McNamara JO (2004) Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43:31-42.
17. Herzog AG, Klein P, Ransil BJ (1997) Three patterns of catamenial epilepsy. Epilepsia 38:1082-1088.
18. Holmes GL, Weber DA (1984) The effect of progesterone on kindling: A developmental study. Brain Res 318:45-53.
19. Hsu SM, Raine L, Fanger H (1981) The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technique. Am J Clin Pathol 75:816-821.
20. Jacobs MP, Leblanc GG, Brooks-Kayal A, Jensen FE, Lowenstein DH, Noebels JL, Spencer DD, Swann JW (2009) Curing epilepsy: Progress and future directions. Epilepsy Behav 14:438-445.
21. Kato J, Hirata S, Nozawa A, Yamada-Mouri N (1994) Gene expression of progesterone receptor isoforms in the rat brain. Horm Behav 28:454-463.
22. 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.
23. Li X, O'Malley BW (2003) Unfolding the actions of progesterone receptors. J Biol Chem 278:39261-39264.
24. Lonsdale D, BurnhamWM (2003) The anticonvulsant effects of progesterone and 5α-dihydroprogesterone on amygdala-kindled seizures in rats. Epilepsia 44:1494-1499.
25. Löscher W (2002) Animal models of epilepsy for the development of antiepileptogenic and disease-modifying drugs.Acomparison of the pharmacology of kindling and post-status epilepticus models of temporal lobe epilepsy. Epilepsy Res 50:105-123.
26. Lothman EW, Williamson JM (1993) Rapid kindling with recurrent hippocampal seizures. Epilepsy Res 14:209-220.
27. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM, O'Malley BW (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278.
28. AR plasticity. Psychoneuroendocrinology 34 [Suppl 1]:S84-S90.
29. A receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8:797-804.
30. Mani S, Portillo W (2010) Activation of progesterone receptors in female reproductive behavior: Interactions with neurotransmitters. Front Neuroendocrinol 31:157-171.
31. Mani SK, Blaustein JD, Allen JM, Law SW, O'Malley BW, Clark JH (1994) Inhibition of rat sexual behavior by antisense oligonucleotides to the progesterone receptor. Endocrinology 135:1409-1414.
32. Mani SK, Allen JM, Lydon JP, Mulac-Jericevic B, Blaustein JD, DeMayo FJ, Conneely O, O'Malley BW (1996) Dopamine requires the unoccupied progesterone receptor to induce sexual behavior in mice. Mol Endocrinol 10:1728-1737.
33. Matsui D, Sakari M, Sato T, Murayama A, Takada I, Kim M, Takeyama K, Kato S (2002) Transcriptional regulation of the mouse steroid 5α- reductase type II gene by progesterone in brain. Nucleic Acids Res 30:1387-1393.
34. McNamara JO, Morrisett R, Nadler JV (1992) Recent advances in understanding mechanisms of the kindling model. Adv Neurol 57:555-560.
35. Mohammad S, Abolhassan A, Pourgholami MH (1998) Evaluation of the anticonvulsant profile of progesterone in male amygdala-kindled rats. Epilepsy Res 30:195-202.
36. Morrell F, deToledo-Morrell L (1999) From mirror focus to secondary epileptogenesis in man: An historical review. Adv Neurol 81:11-23.
37. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM (2000) Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751-1754.
38. Parsons B, Rainbow TC, MacLusky NJ, McEwen BS (1982) Progestin receptor levels in rat hypothalamic and limbic nuclei. J Neurosci 2:1446-1452. (Pubitemid 13255862)
39. Persad V, Ting Wong CG, Cortez MA, Wang YT, Snead OC 3rd (2004) Hormonal regulation of atypical absence seizures. Ann Neurol 55:353-361.
40. Pitkänen A, Immonen RJ, Gröhn OH, Kharatishvili I (2009) From traumatic brain injury to posttraumatic epilepsy: What animal models tell us about the process and treatment options. Epilepsia 50 [Suppl 2]:21-29.
41. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
42. Reddy DS (2009) The role of neurosteroids in the pathophysiology and treatment of catamenial epilepsy. Epilepsy Res 85:1-30.
43. A receptors. J Pharmacol Exp Ther 334:1031-1041.
44. Reddy DS, Mohan A (2010) Progesterone receptor-mediated seizure susceptibility in female mice. Soc Neurosci Abstr 36:255.12.
45. Reddy DS, Kim HY, Rogawski MA (2001) Neurosteroid withdrawal model of perimenstrual catamenial epilepsy. Epilepsia 42:328-336.
46. Reddy DS, Castaneda DC, O'Malley BW, RogawskiMA (2004) Anticonvulsant activity of progesterone and neurosteroids in progesterone receptor knockout mice. J Pharmacol Exp Ther 310:230-239.
47. Reddy DS, O'Malley BW, Rogawski MA (2005a) Anxiolytic activity of progesterone in progesterone receptor knockout mice. Neuropharmacology 48:14-24.
48. Reddy DS, Venkatarangan L, Chien B, Ramu K (2005b) A high-performance liquid chromatography-tandem mass spectrometry assay of the androgenic neurosteroid 3α-androstanediol in plasma. Steroids 70:879-885.
49. Reddy DS, Gangisetty O, Briyal S (2010) Disease-modifying activity of progesterone in the hippocampus kindling model of epileptogenesis. Neuropharmacology 59:573-581.
50. Rupprecht R, Reul JM, Trapp T, van Steensel B, Wetzel C, Damm K, Zieglgänsberger W, Holsboer F (1993) Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11:523-530.
51. Sankar R, Auvin S, Kwon YS, Pineda E, Shin D, Mazarati A (2010) Evaluation of development-specific targets for antiepileptogenic therapy using rapid kindling. Epilepsia 51 [Suppl 3]:39-42.
52. Scharfman HE, MacLusky NJ (2006) The influence of gonadal hormones on neuronal excitability, seizures, and epilepsy in the female. Epilepsia 47:1423-1440.
53. Silver JM, Shin C, McNamara JO (1991) Antiepileptogenic effects of conventional anticonvulsants in the kindling model of epilepsy. Ann Neurol 29:356-363.
54. Talmi M, Carlier E, Bengelloun W, Soumireu-Mourat B (1995) Synergistic action of corticosterone on kainic acid-induced electrophysiological alterations in the hippocampus. Brain Res 704:97-102.
55. Walker MC, White HS, Sander JW (2002) Disease modification in partial epilepsy. Brain 125:1937-1950.
56. Zhou QX, Mao RR, Duan TT, Tan JW, Tian M, Cao J, Xu L (2010) Stress within the postseizure time window inhibits seizure recurrence. Epilepsy Behav 18:201-206.