Effect of hormonal replacement therapy in the hippocampus of ovariectomized epileptic female rats using the pilocarpine experimental model

Epilepsy Research

Volumn 82, Issue 1, 2008, Pages 46-56

  Valente, S G ^a,d   Marques, R H ^e   Baracat, E C ^b   Cavalheiro, E A ^a   Naffah Mazzacoratti, M G ^c   Amado, D ^a  

^a Neurocirurgia Disciplina de Neurologia Experimental   (Brazil)

^b Santa Casa de Misericórdia de São Paulo   (Brazil)

^c Unicamp   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e Núcleo de Pesquisa em Fisiologia Médica Centro Universitário Lusíada   (Brazil)

Author keywords

Epilepsy; Hippocampus; Ovariectomy; Pilocarpine and Hormonal replacement therapy

Indexed keywords

ESTRADIOL; MEDROXYPROGESTERONE; PILOCARPINE; SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EPILEPTIC STATE; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; HORMONE SUBSTITUTION; MORBIDITY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; ANIMAL; CHEMICALLY INDUCED DISORDER; COMPARATIVE STUDY; ESTRUS; GENERALIZED EPILEPSY; HYPOGONADISM; PATHOPHYSIOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; EPILEPSY, GENERALIZED; ESTRADIOL; ESTRUS; FEMALE; GONADAL STEROID HORMONES; HIPPOCAMPUS; HORMONE REPLACEMENT THERAPY; HYPOGONADISM; MEDROXYPROGESTERONE; MOSSY FIBERS, HIPPOCAMPAL; OVARIECTOMY; PILOCARPINE; RATS; RATS, WISTAR;

EID: 64149089930     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2008.07.003     Document Type: Article

References (70)

1. Agresti A. Categorical Data Analysis. second ed. (2002), John Wiley & Sons, New York
2. Allen E., and Doisy E.A. Ovarian and placental hormones. Physiol. Rev. 7 (1923) 600-650
3. Amado D., and Cavalheiro E.A. Hormonal and gestational parameters in female rats submitted to the pilocarpine model of epilepsy. Epilepsy Res. 32 (1998) 266-274
4. Amado D., Cavalheiro E.A., and Bentivoglio M. Epilepsy and hormonal regulation: the pattern of GnRh and galanin immunoreactivity in the hypothalamus of epileptic female rat. Epilepsy Res. 14 (1993) 149-159
5. Backstrom T., and Rosciszewska D. Effects of hormones on seizures expression. In: Engel Jr. J., and Pedley T.A. (Eds). Epilepsy: A Comprehensive Textbook (1997), Lippincott Raven, Philadelphia 2003-2012
6. Behr J., Lyson K.J., and Mody I. Enhanced propagation of epileptiform activity through the kindled dentate gyrus. J. Neurophysiol. 79 (1998) 1726-1732
7. Bilo L., Meo R., Nappi C., Annunziato L., Striano S., Colao A.M., Merola B., and Buscaino G.A. Reproductive endocrine disorders in women with primary generalized epilepsy. Epilepsy 29 (1988) 612-619
8. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., and Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 32 (1991) 778-782
9. CIOMS/OMS. International Guiding Principles for Biomedical Research Involving Animals (1985), Council for International Organizations of Medical Services. WHO Distribution and Sales Service, 1211 Geneva 27, Switzerland
10. Clauberg C. Das Hormon des corpus luteum. Zentr. Gynäk. 54 (1930) 2757
11. Cramer J.A., and Jones E.E. Reproductive function in epilepsy. Epilepsia 32 6 (1991) S19-S26
12. Cummings L.N., Giudice L., and Morrell M.J. Ovulatory function in epilepsy. Epilepsia 36 (1995) 353-357
13. Diamantopoulos N., and Crumrine P.K. The effect of puberty on the course of epilepsy. Arch. Neurol. 43 (1986) 873-876
14. Edwards D.P. Regulation of signal transduction pathways by estrogen and progesterone. Annu. Rev. Physiol. 67 (2005) 335-376
15. Edwards H.E., Epps T., Carlen P.L., and MacLusky N.J. Progestin receptors mediate progesterone suppression of epileptiform activity in tetanized hippocampal slices in vitro. Neuroscience 101 4 (2000) 895-906
16. Edwards H.E., Burnham W.M., Mendonca A., Bowlby D.A., and MacLusky N.J. Steroid hormones affect limbic after discharge thresholds and kindling rates in adult female rats. Brain Res. 838 (1999) 136-150
17. El Bahh B., Balosso S., Hamilton T., Herzog H., Beck-Sickinger A.G., Sperk G., et al. The anti-epileptic actions of neuropeptide Y in the hippocampus are mediated by Y2 and not Y5 receptors. Eur. J. Neurosci. 22 (2005) 1417-1430
18. Foldvary-Schaefer N., Harden C., Herzog A., and Falcone T. Hormones and seizures. Cleveland Clin. J. Med. 71 Suppl. 2 (2004) S11-S18
19. Freund T.F., and Buzsaki G. Interneuron of the hippocampus. Hippocampus 6 (1996) 347-470
20. Galanopoulou A.S., Alm E.M., and Velisková J. Estradiol reduces seizures-induced hippocampal injury in ovariectomized female but not in male rats. Neurosci. Lett. 342 (2003) 201-205
21. Garcia-Segura L.M., Azcoitia I., and Don Carlos L.L. Neuroprotection by estradiol. Prog. Neurobiol. 63 (2001) 29-60
22. Herzog A.G. A hypothesis to integrate partial seizures of temporal lobe origin and reproductive endocrine disorder. Epilepsy Res. 3 (1989) 151-159
23. Herzog A.G., Seibel M.M., Schomer D.L., Vaitukaitis J.L., and Geschwind N. Reproductive endocrine disorders in women with partial seizures of temporal lobe origin. Arch. Neurol. 43 (1986) 341-346
24. Herzog A.G. Progesterone therapy in women with complex partial and secondary generalized seizures. Neurology 45 (1995) 1660-1662
25. Herzog A.G. Progesterone therapy in women with epilepsy: a 3-year follow-up. Neurology 52 (1999) 1917-1918
26. Herzog A.G. Psychoneuroendocrine aspects of temporolimbic epilepsy. Part I. Brain, reproductive steroids and emotions. Psychosomatics 40 (1999) 95-101
27. Herzog A.G. Intermittent progesterone therapy and frequency of complex partial seizures in women with menstrual disorders. Neurology 36 (1986) 1607-1610
28. Hoffman G.E., Moore N., Fiskum G., and Murphy A.Z. Ovarian steroids modulation of seizures severity and hippocampal cell death after kainic acid treatment. Exp. Neurol. 182 (2003) 124-134
29. Isojärvi J.I.T., Laatikainen T.J., Pakarinen A.J., Juntunen K.T.S., and Myllyla V.V. Polycystic ovaries and hyperandrogenism in women taking valproate for epilepsy. N. Engl. J. Med. 329 (1993) 1383-1388
30. Jacono J.J., and Robertson J.M.D. The effect of estrogen, progesterone, and ionized calcium on seizures during the menstrual cycle of epileptic women. Epilepsia 28 (1987) 571-577
31. Joels M. Steroids hormones and excitability in the mammalian brain. Front. Neuroendocrinol. 18 (1997) 2-48
32. Kokate T.G., Banks M.K., Magee T., Yamaguchi S., and Rogawski M.A. Finasteride, a 5(-reductase inhibitor, blocks the anticonvulsant activity of progesterone in mice. J. Pharmacol. Exp. Ther. 288 (1999) 679-684
33. Landgren S., Aasly J., Bäckströn T., Dubrovsky B., and Danielson E. The effects of progesterone and its metabolites on the interictal epileptiform discharge in the cat's cerebral cortex. Acta Physiol. Scand. 131 (1987) 33-42
34. Lephart E.D. Brain 5(-reductase: cellular, enzymatic, and molecular perspective and implications for biological function. Mol. Cell. Neurosci. 4 (1993) 473-484
35. Li C., Brake W.G., Romeo R.D., et al. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2185-2219
36. MacLusky N.J., Luine V.N., Hajszan T., et al. The 17( and 17( isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 146 (2005) 287-293
37. Manthey D., and Behl C. From structural biochemistry to expression profiling: neuroprotective activities of estrogen. Neuroscience 138 (2006) 845-850
38. Mathern G.M., Babb T.L., Pretorius J.K., and Leite J.P. Reactive synaptogenesis and neuron density for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentate. J. Neurosci. 15 (1995) 3990-4004
39. Mathern G.M., Babb T.L., and Mischel P.S. Childhood generalized and mesial temporal epilepsies demonstrate different amounts and patterns of hippocampal neuron loss and mossy fiber synaptic reorganization. Brain 119 (1996) 965-987
40. Mattson R.H., Cramer J.A., Caldwell B., and Siconolfi B. Treatment of seizures with medroxyprogesterone acetate: preliminary report. Neurology 34 (1984) 1255-1258
41. McEwen B.S., and Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 20 (1999) 279-307
42. McGinnis M.Y., MacLusky N.J., and McEwen B.S. Steroid receptor levels in intact and ovariectomized estrogen-treated rats: an examination of quantitative, temporal and endocrine related factors influencing the efficacy of an estradiol stimulus. Neuroendocrinology 33 (1981) 158-165 EMBASE
43. Morrell M.J. Sexual dysfunction in epilepsy. Epilepsia 32 Suppl. 6 (1991) S38-S45
44. Morrell M.J. Epilepsy in women: the science of why it is special. Neurology 53 4 Suppl. 1 (1999) S42-S48
45. Morrell M.J., Flynn K.L., Done S., Flaster E., Kalayjian L., and Pack A.M. Sexual dysfunction, sex steroids hormones abnormalities, and depression in women with epilepsy treated with antiepileptic drugs. Epilepsy Behav. 6 3 (2005) 360-365
46. Okasaki M.M., Evenson D.A., and Nadler J.V. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J. Comp. Neurol. 352 (1995) 515-534
47. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, Orlando, FL
48. Pitkänen A., Nissinen J., Lukasiuk K., Jutila L., Paljärvi L., Salmenperä T., Karkola K., Vapalahti M., and Ylinen A. Association between the density of mossy fiber sprouting and seizures frequency in experimental and human temporal lobe epilepsy. Epilepsia 41 Suppl. 6 (2000) S24-S29
49. Reibel S., Andre V., Chassagnon S., Andre G., Marescaux C., and Nehlig A. Neuroprotective effects of chronic estradiol benzoate treatment on hippocampal cell loss induced by status epilepticus in the female rat. Neurosci. Lett. 281 (2000) 79-82
50. Roscizewska D., Butner B., Guz I., and Zawisza L. Ovarian hormones, anticonvulsant drugs and seizures during the menstrual cycle in women with epilepsy. J. Neurol. Neurosurg. Psych. 49 (1986) 47-51
51. Rudick C.N., and Woolley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J. Neurosci. 21 (2001) 6532-6543
52. Scharfman H.E., and MacLusky N.J. The influence of gonadal hormones on neuronal excitability, seizures, and epilepsy in the female. Epilepsia 47 9 (2006) 1423-1440
53. Scharfman H.E., Goodman J.H., Rigoulot M.A., Berger R.E., Walling S.G., Mercurio T.C., Stormes K., and Maclusky N.J. Seizure susceptibility in intact and ovariectomized female rats treated with the convulsant pilocarpine. Exp. Neurol. 196 (2005) 73-86
54. Segal M., and Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm. Behav. 40 (2001) 156-159
55. Smith S.S., Waterhouse B.D., and Woodward D.J. Locally applied progesterone metabolites alter neuronal responsiveness in the cerebellum. Brain Res. Bull. 18 (1987) 739-747
56. Sperk G., Marksteiner J., Gruber B., Bellmann R., Mahata M., and Ortler M. Functional changes in neuropeptide Y and somastotatin-containing neuron induced by limbic seizures in the rat. Neuroscience 50 (1992) 831-846
57. Stuenkel C.A. Neural regulation of pituitary function. Epilepsia 32 Suppl. 6 (1991) S2-S10
58. Tauck D.L., and Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5 (1985) 1016-1022
59. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., and Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 9 (1983) 315-335
60. Valente S.G., Naffah-Mazzacoratti M.G., Pereira M., Silva I., Santos N.F., Baracat E.C., Cavalheiro E.A., and Amado D. Castration in female rats modifies the development of pilocarpine model of epilepsy. Epilepsy Res. 49 (2002) 181-188
61. Van de Pol N.E., and Van Goozen S.H.M. Hypothalamic involvement in sexuality and hostility: comparative psychological aspects. Prog. Brain Res. 93 3 (1992) 43-361
62. Velisková J., Velisek L., Galanopoulou A.S., and Sperber E.F. Neuroprotetive effects of estrogens on hippocampal cells in adult female rats after status epilepticus. Epilepsia 41 Suppl. 6 (2000) S30-S35
63. Velisková J. The role of estrogens in seizures and epilepsy: the bad guys or the good guys?. Neuroscience 138 (2006) 837-844
64. Webber M.P., Hauser W.A., Ottman R., and Annergers J.F. Fertility in person with epilepsy. Epilepsia 27 (1986) 746-752
65. Weiland N.G. Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus. Endocrinology 131 (1992) 2697-2702
66. Winner B.J. Statistical Principles in Experimental Design. second ed. (1971), McGraw-Hill, Tokyo
67. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12 7 (1992) 2549-2554
68. Woolley D.E., and Timiras P.S. The gonad-brain relationship: effects of female sex hormones on electroshock convulsions in the rats. Endocrinology 70 (1962) 196-209
69. Zamani M.R., Levy W.B., and Desmond N.L. Estradiol increases delayed, N-methyl-d-aspartate receptor-mediated excitation in the hippocampal CA1 region. Neuroscience 129 (2004) 243-254
70. Zimmerman A.W., Holder D.T., Reiter E.O., and Dekaban A.S. Medroxyprogesterone acetate in the treatment of seizures associated with menstruation. J. Pediatr. 83 (1973) 959-963