Effects of 17β-estradiol replacement on the apoptotic effects caused by ovariectomy in the rat hippocampus

Life Sciences

Volumn 86, Issue 21-22, 2010, Pages 832-838

  Sales, Sayuri ^a   Ureshino, Rodrigo Portes ^b   Pereira, Renato Tavares dos Santos ^a   Luna, Milene Schmidt Amaral ^a   Pires de Oliveira, Marcelo ^b   Yamanouye, Norma ^a   Godinho, Rosely Oliveira ^b   Smaili, Soraya Soubhi ^b   Porto, Catarina Segreti ^b   Abdalla, Fernando Maurício Francis ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

17 estradiol; Bax; Bcl 2; Hippocampus; Ovariectomy

Indexed keywords

ESTRADIOL; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HIPPOCAMPUS; HORMONE SUBSTITUTION; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; PROESTRUS; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; CHEMISTRY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

RATTUS;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; ESTRADIOL; FEMALE; HIPPOCAMPUS; OVARIECTOMY; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR;

EID: 77952673040     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2010.04.002     Document Type: Article

References (75)

1. Alkayed N.J., Goto S., Sugo N., Joh H.D., Klaus J., Crain B.J., Bernard O., Traystman R.J., Hum P. Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. The Journal of Neuroscience 2001, 21:7543-7550.
2. Azcoitia I., Sierra A., Garcia-Segura L.M. Neuroprotection effects of estradiol in the adult rat hippocampus: interaction with insulin-like growth factor-I signaling. Journal of Neuroscience Research 1999, 58:815-822.
3. Bagetta G., Chiappetta O., Amantea D., Iannone M., Rotiroti D., Costa A., Nappi G., Corasaniti M.T. Estradiol reduces cytochrome c translocation and minimizes hippocampal damage caused by transient global ischemia in rat. Neuroscience Letters 2004, 368:87-91.
4. Barha C.K., Galea L.A. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochimica et Biophysica Acta 2010, 10.1016/j.bbagen.2010.01.006.
5. Barha C.K., Lieblich S.E., Galea L.A. Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. Journal of Neuroendocrinology 2009, 21:155-166.
6. Behl C., Widmann M., Trapp T., Holsboer F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochemical & Biophysical Research Communications 1995, 216:473-482.
7. Brann D.W., Dhandapani K., Wakade C., Mahesh V.B., Khan M.M. Neurotrophic and neuroprotective actions of estrogens: basic mechanisms and clinical implications. Steroids 2007, 72:381-405.
8. Cardoso C.C., Pereira R.T.S., Koyama C.A., Porto C.S., Abdalla F.M.F. Effect of estrogen on muscarinic acetylcholine receptors in rat hippocampus. Neuroendocrinology 2004, 80:379-386.
9. Carvalho F.F., Nencioni A.L., Lebrun I., Sandoval M.R., Dorce V.A. Behavioral, electroencephalographic, and histopathologic effects of a neuropeptide isolated from Tityus serrulatus scorpion venom in rats. Pharmacology Biochemistry & Behavior 1998, 60:7-14.
10. Choi Y.C., Lee J.H., Hong K.W., Lee K.S. 17 Beta-estradiol prevents focal cerebral ischemic damages via activation of Akt and CREB in association with reduced PTEN phosphorylation in rats. Fundamental & Clinical Pharmacology 2004, 18:547-557.
11. Cornil C.A., Ball G.F., Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from?. Brain Research 2006, 1126:2-26.
12. Cregan S.P., Fortin A., MacLaurin J.G., Callaghan S.M., Cecconi F., Yu S.W., Dawson T.M., Dawson V.L., Park D.S., Kroemer G., Slack R.S. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. The Journal of Cell Biology 2002, 158:507-517.
13. Daniel J.M., Hulst J.L., Berbling J.L. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 2006, 147:607-614.
14. Desagher S., Martinou J.C. Mitochondria as the central control point of apoptosis. Trends in Cell Biology 2000, 10:369-377.
15. Dubal D.B., Kashon M.L., Pettigrew L.C., Ren J.M., Finklestein S.P., Rau S.W., Wise P.M. Estradiol protects against ischemic injury. Journal of Cerebral Blood Flow & Metabolism 1998, 18:1253-1258.
16. Dubal D.B., Shughrue P.J., Wuison M.E., Merchenthaler I., Wise P.M. Estradiol modulates Bcl-2 in cerebral ischemia: a potential role for estrogen receptors. The Journal of Neuroscience 1999, 19:6385-6393.
17. Everett J.W. Progesterone and estrogen in the experimental control of ovulation time and other features of the estrous cycle in the rat. Endocrinology 1948, 43:389-405.
18. Forger N.G. Cell death and sexual differentiation of the nervous system. Neuroscience 2006, 138:929-938.
19. Foster T.C. Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Frontiers in Neuroendocrinology 2005, 26:51-64.
20. Garcia-Segura L.M., Cardona-Gomez P., Naftolin F., Chowen J.A. Estradiol up-regulates Bcl-2 expression in adult brain neurons. NeuroReport 1998, 9:593-597.
21. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. The Journal of Cell Biology 1992, 119:493-501.
22. Gibbs R.B. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Research 1997, 757:10-16.
23. Gibbs R.B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Experimental Neurology 1998, 151:289-302.
24. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiology of Aging 2000, 21:107-116.
25. Gold R., Schmied M., Giegerich G., Breitschopf H., Hartung H.P., Toyka K.V., Lassmann H. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Laboratory Investigation 1994, 71:219-225.
26. Goodman Y., Bruce A.J., Cheng B., Mattson M.P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. Journal of Neurochemistry 1996, 66:1836-1844.
27. Green P.S., Gridley K.E., Simpkins J.W. Estradiol protects against beta-amyloid (25-35)-induced toxicity in SK-N-SH human neuroblastoma cell. Neuroscience Letters 1996, 218:165-168.
28. Green P.S., Bishop J., Simpkins J.W. 17 alpha-estradiol exerts neuroprotective effects on SK-N-SH cells. The Journal of Neuroscience 1997, 17:511-515.
29. Iwasaki K., Hatip-Al-Khatib I., Egashira N., Akiyoshi Y., Arai T., Mishima K., Takagaki Y., Inui K., Fujiwara M. Ovariectomy combined with amyloid beta(1-42) impairs memory by decreasing acetylcholine release and alpha 7nAChR expression without induction of apoptosis in the hippocampus CA1 neurons of rats. Neurotoxicity Research 2004, 6:299-309.
30. Jover-Mengual T., Zukin R.S., Etgen A.M. MAPK signaling is critical to estradiol protection of CA1 neurons in global ischemia. Endocrinology 2007, 148:1131-1143.
31. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nature Medicine 2000, 6:513-519.
32. Lankiewicz S., Luetjens M.C., Bui T.N., Krohn A.J., Poppe M., Cole G.M., Saido T.C., Prehn J.H. Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. Journal of Biology Chemistry 2000, 275:17064-17071.
33. Li L.Y., Luo X., Wang X. Endonuclease G in an apoptotic DNase when released from mitochondria. Nature 2001, 412:95-99.
34. Lovekamp-Swan T., Glendenning M.L., Schreihofer D.A. A high soy diet enhances neurotropin receptor and Bcl-XL gene expression in the brains of ovariectomized female rats. Brain Research 2007, 1159:54-66.
35. McCullough L.D., Alkayed N.J., Traystman R.J., Williams M.J., Hurn P.D. Postischemic estrogen reduces hypoperfusion and secondary ischemic after experimental stroke. Stroke 2001, 32:796-802.
36. McEwen B. Estrogen actions throughout the brain. Recent Progress in Hormone Research 2002, 57:357-384.
37. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocrine Reviews 1999, 20:279-307.
38. Mehra R.D., Sharma K., Nyakas C., Kij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Research 2005, 1056:22-35.
39. Mook-Jung I., Jo I., Sohn S., Kwon H.J., Huh K., Jung M.W. Estrogen blocks neurotoxic effects of beta-amyloid (1-42) and induces neurite extension on B103 cells. Neuroscience Letters 1997, 235:101-104.
40. Nequin L.G., Alvarez J., Schwartz N.B. Measurement of serum steroid and gonadotropin levels and uterine and ovarian variables throughout 4day and 5day estrous cycles in the rat. Biology of Reproduction 1979, 20:659-670.
41. Nunez J.L., McCarthy M.M. Cell death in the rat hippocampus in a model of prenatal brain injury: time course and expression of death-related proteins. Neuroscience 2004, 129:393-402.
42. Penninger J.M., Kroemer G. Mitochondria, AIF and caspases-rivaling for cell death execution. Nature Cell Biology 2003, 5:97-99.
43. Pereira R.T.S., Porto C.S., Godinho R.O., Abdalla F.M.F. Effects of estrogen on intracellular signaling pathways linked to activation of muscarinic acetylcholine receptors and on acetylcholinesterase activity in rat hippocampus. Biochemical Pharmacology 2008, 75:1827-1834.
44. Pike C.J. Estrogen modulates neuronal Bcl-xL expression and β-amyloid-induced apoptosis: relevance to Alzheimer's disease. Journal of Neurochemistry 1999, 72:1552-1563.
45. Rau S.W., Dubal D.B., Bottner M., Gerhold L.M., Wise P.M. Estradiol attenuates programmed cell death after stroke-like injury. The Journal of Neuroscience 2003, 23:11420-11426.
46. Saleh A., Srinivasula S.M., Acharya S., Fishel R., Alnemri E.S. Citochrome and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. Journal of Biological Chemistry 1999, 274:17941-17945.
47. Sharma K., Mehra R.D. Long-term administration of estrogen or tamoxifen to ovariectomized rats affords neuroprotection to hippocampal neurons by modulating the expression of Bcl-2 and Bax. Brain Research 2008, 1204:1-15.
48. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and-beta mRNA in the rat central nervous system. The Journal of Comparative Neurology 1997, 388:507-525.
49. Simpkins J.W., Rajakumar G., Zhang Y.Q., Simpkins C.E., Greenwald D., Yu C.J., Bodor N., Day A.L. Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. Journal of Neurosurgery 1997, 87:724-730.
50. Singer C.A., Rogers K.L., Dorsa D.M. Modulation of Bcl-2 expression: a potential component of estrogen neuroprotection. NeuroReport 1998, 9:2565-2568.
51. Snedecor G.W., Cochran W.G. Statistical Methods 1980, 89-233. Iowa State University Press, Ames USA. 7th edn.
52. Soustiel J.F., Palzier E., Nevo O., Thaler I., Vlodavsky E. Neuroprotective anti-apoptosis effect of estrogens in traumatic brain injury. Journal of Neurotrauma 2005, 22:345-352.
53. Stoltzner S.E., Berchtold N.C., Cotman C.W., Pike C.J. Estrogen regulates Bcl-x expression in rat hippocampus. NeuroReport 2001, 12:2797-2800.
54. Strasser A., Harris A.W., Hwang D.C., Krammer P.H., Cory S. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. The EMBO Journal 1995, 14:6136-6147.
55. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
56. Tanapat P., Hastings N.B., Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. The Journal of Comparative Neurology 2005, 481:252-265.
57. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science 1998, 281:1312-1316.
58. Toran-Allerand C.D. Estrogen and the brain: BEYOND ER-{alpha}, ER-{beta}, and 17{beta}-Estradiol. Annals of the New York Academy of Sciences 2005, 1052:136-144.
59. Varfolomeev E.E., Schuchmann M., Lurca V., Chiannilkulchai N., Beckmann J.S., Mett I.L., Rebrikov D., Brodianski V.M., Kemper O.C., Kollet O., Lapidot T., Soffer D., Sobe T., Avraham K.B., Goncharov T., Holtmann H., Lonai P., Wallach D. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/APO 1, and DR3 and is lethal prenatally. Immunity 1998, 9:267-276.
60. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
61. Villa P.G., Henzel W.J., Sensenbrenner M., Henderson C.E., Pettmann B. Calpain inhibitors, but not caspase inhibitors, prevent actin proteolysis and DNA fragmentation during apoptosis. Journal of Cell Science 1998, 111:713-722.
62. Wang X. The expanding role of mitochondria in apoptosis. Genes & Development 2001, 15:2922-2933.
63. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Bottner M., Rosewell K.L. Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Research Reviews 2001, 37:313-319.
64. Wolf B.B., Goldstein J.C., Stennicke H.R., Beere H., Amarante-Mendes G.P., Salvesen G.S., Green D.R. Calpain functions in a caspase-independent manner to promote apoptotic-like events during platelet activation. Blood 1999, 94:1683-1692.
65. Won C.K., Kim M.O., Koh P.O. Estrogen modulates Bcl-2 family proteins in ischemic brain injury. The Journal of Veterinary Medical Science 2006, 68:277-280.
66. Woolley C.S., McEwen B. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. The Journal of Comparative Neurology 1993, 336:293-306.
67. Wu T.W., Wang J.M., Chen S., Brinton R.D. 17β-estardiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and Bcl-2 expression in rat hippocampal neurons: a potential initiation mechanisms for estrogen-induced neuroprotection. Neuroscience 2005, 135:59-72.
68. Xiang J., Chao D.T., Korsmeyer S.J. Bax induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proceedings of the National Academic of Sciences of the United States of America 1996, 93:14559-14563.
69. Yang S.H., Shi J., Day A.L., Simpkins J.W. Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 2000, 31:745-749.
70. Yang S.H., Liu R., Wu S.S., Simpkins J.W. The use of estrogens and related compounds in the treatment of damage from cerebral ischemia. Annals of the New York Academy of Sciences 2003, 1007:101-107.
71. Yao M., Nguyen T.V., Pike C.J. Estrogen regulates Bcl-w and Bim expression: role in protection against beta-amyloid peptide-induced neuronal death. The Journal of Neuroscience 2007, 27:1422-1433.
72. Yune T.Y., Kim S.J., Lee S.M., Lee Y.K., Oh Y.J., Kim Y.C., Markelonis G.J., Oh T.H. Systemic administration of 17 beta-estradiol reduces apoptotic cell death and improves functional recovery following traumatic spinal cord injury in tars. Journal of Neurotrauma 2004, 21:293-306.
73. Zhang L., Nair A., Krady K., Corpe C., Bonneau R.H., Simpson I.A., Vannucci S.J. Estrogen stimulates microglia and brain recovery from hypoxia-ischemia in normoglycemic but not diabetic female mice. The Journal of Clinical Investigation 2004, 113:85-95.
74. Zhao L., Wu T.W., Brinton R.D. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Research 2004, 1010:22-34.
75. Zhao S., Konopleva M., Cabreira-Hansen M., Xie Z., Hu W., Milella M., Estrov Z., Mills G.B., Andreeff M. Inhibition of phosphatidylinositol 3-kinase dephosphorylates BAD and promotes apoptosis in myeloid leukemias. Leukemia 2004, 18:267-275.