Long-term ovariectomy increases BDNF gene methylation status in mouse hippocampus

Journal of Steroid Biochemistry and Molecular Biology

Volumn 144, Issue PART B, 2014, Pages 243-252

  Moreno Piovano, Guillermo S ^a   Varayoud, Jorgelina ^a   Luque, Enrique H ^a   Ramos, Jorge G ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Brain derived neurotrophic factor; DNA methylation; Estrogen; Hippocampus

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; SYNAPTOPHYSIN; SYP PROTEIN, MOUSE;

ANIMAL; BAGG ALBINO MOUSE; BLOOD; DNA METHYLATION; DRUG ADMINISTRATION; DRUG EFFECTS; FEMALE; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; HIPPOCAMPUS; METABOLISM; OVARIECTOMY; PROMOTER REGION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA METHYLATION; DRUG ADMINISTRATION SCHEDULE; EPIGENESIS, GENETIC; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HIPPOCAMPUS; MICE, INBRED BALB C; OVARIECTOMY; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SYNAPTOPHYSIN; TRANSCRIPTION, GENETIC;

EID: 84906839043     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.08.001     Document Type: Article

References (71)

1. V.W. Henderson Estrogen, cognition, and a woman's risk of Alzheimer's disease Am. J. Med. 103 1997 11S 18S (Pubitemid 27444160)
2. C. Kawas, S. Resnick, A. Morrison, R. Brookmeyer, M. Corrada, A. Zonderman, C. Bacal, D.D. Lingle, and E. Metter A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging Neurology 48 1997 1517 1521
3. A. Paganini-Hill Estrogen replacement therapy and stroke Prog. Cardiovasc Dis. 38 1995 223 242
4. J.M. Daniel Estrogens, estrogen receptors, and female cognitive aging: the impact of timing Horm. Behav. 63 2013 231 237
5. P.R. Moult, and J. Harvey Hormonal regulation of hippocampal dendritic morphology and synaptic plasticity Cell Adhes. Migr. 2 2008 269 275
6. M.R. Foy, M. Baudry, G.K. Akopian, and R.F. Thompson Regulation of hippocampal synaptic plasticity by estrogen and progesterone Vitam. Horm. 82 2010 219 239
7. T. Numakawa, S. Suzuki, E. Kumamaru, N. Adachi, M. Richards, and H. Kunugi BDNF function and intracellular signaling in neurons Histol. Histopathol. 25 2010 237 258
8. J.D. Gray, T.A. Milner, and B.S. McEwen Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors Neuroscience 239 2013 214 227
9. K. Yamada, M. Mizuno, and T. Nabeshima Role for brain-derived neurotrophic factor in learning and memory Life Sci. 70 2002 735 744 (Pubitemid 34075562)
10. M.J. Schaaf, J.O. Workel, H.M. Lesscher, E. Vreugdenhil, M.S. Oitzl, and E.R. de Kloet Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats Brain Res. 915 2001 227 233 (Pubitemid 32947038)
11. M.G. Murer, Q. Yan, and R. Raisman-Vozari Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease Prog. Neurobiol. 63 2001 71 124
12. M. Takahashi, O. Shirakawa, K. Toyooka, N. Kitamura, T. Hashimoto, K. Maeda, S. Koizumi, K. Wakabayashi, H. Takahashi, T. Someya, and H. Nawa Abnormal expression of brain-derived neurotrophic factor and its receptor in the corticolimbic system of schizophrenic patients Mol. Psychiatry 5 2000 293 300 (Pubitemid 30438405)
13. G. Schlaf, C. Salje, R. Poethke, K. Felgenhauer, and M. Mader A novel enzyme-linked immunosorbent assay for determination of synaptophysin as compared with other quantification procedures J. Neuroimmunol. 67 1996 59 65 (Pubitemid 26245704)
14. J.E. Gresack, and K.M. Frick Environmental enrichment reduces the mnemonic and neural benefits of estrogen Neuroscience 128 2004 459 471 (Pubitemid 39277418)
15. R.B. Gibbs Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement Brain Res. 810 1998 294
16. H.E. Scharfman, T.C. Mercurio, J.H. Goodman, M.A. Wilson, and N.J. MacLusky Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor J. Neurosci. 23 2003 11641 11652 (Pubitemid 38021291)
17. H.E. Scharfman, T.M. Hintz, J. Gomez, K.A. Stormes, S. Barouk, G.H. Malthankar-Phatak, D.P. McCloskey, V.N. Luine, and N.J. Maclusky Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge Eur. J. Neurosci. 26 2007 2595 2612 (Pubitemid 350050429)
18. M. Singh, E.M. Meyer, and J.W. Simpkins The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats Endocrinology 136 1995 2320 2324
19. D.D. Murphy, N.B. Cole, and M. Segal Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons Proc. Natl. Acad. Sci. U. S. A. 95 1998 11412 11417 (Pubitemid 28450142)
20. R.B. Gibbs Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain Brain Res. 844 1999 20 27 (Pubitemid 29490948)
21. I. Cavus, and R.S. Duman Influence of estradiol, stress, and 5-HT2A agonist treatment on brain-derived neurotrophic factor expression in female rats Biol. Psychiatry 54 2003 59 69 (Pubitemid 36776724)
22. N.C. Berchtold, J.P. Kesslak, C.J. Pike, P.A. Adlard, and C.W. Cotman Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus Eur. J. Neurosci. 14 2001 1992 2002 (Pubitemid 35463686)
23. M. Day, and M. Good Ovariectomy-induced disruption of long-term synaptic depression in the hippocampal CA1 region in vivo is attenuated with chronic estrogen replacement Neurobiol. Learn. Mem. 83 2005 13 21 (Pubitemid 40018022)
24. B.B. Sherwin Estrogen and memory in women: how can we reconcile the findings? Horm. Behav. 47 2005 371 375 (Pubitemid 40222746)
25. T. Timmusk, K. Palm, M. Metsis, T. Reintam, V. Paalme, M. Saarma, and H. Persson Multiple promoters direct tissue-specific expression of the rat BDNF gene Neuron 10 1993 475 489 (Pubitemid 23111738)
26. F. Sohrabji, R.C. Miranda, and C.D. Toran-Allerand Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor Proc. Natl. Acad. Sci. U. S. A. 92 1995 11110 11114
27. K. Martinowich, D. Hattori, H. Wu, S. Fouse, F. He, Y. Hu, G. Fan, and Y.E. Sun DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation Science 302 2003 890 893 (Pubitemid 37339633)
28. N.M. Tsankova, O. Berton, W. Renthal, A. Kumar, R.L. Neve, and E.J. Nestler Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action Nat. Neurosci. 9 2006 519 525
29. R.B. Gibbs Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats Neurobiol. Aging 21 2000 107 116 (Pubitemid 30224792)
30. V.L. Bosquiazzo, J.G. Ramos, J. Varayoud, M. Munoz-de-Toro, and E.H. Luque Mast cell degranulation in rat uterine cervix during pregnancy correlates with expression of vascular endothelial growth factor mRNA and angiogenesis Reproduction 133 2007 1045 1055 (Pubitemid 47162594)
31. R. Higuchi, C. Fockler, G. Dollinger, and R. Watson Kinetic PCR analysis: real-time monitoring of DNA amplification reactions Biotechnology 11 1993 1026 1030 (Pubitemid 23254023)
32. J. Varayoud, L. Monje, G.S. Moreno-Piovano, G.H. Galoppo, E.H. Luque, M. Munoz-de-Toro, and J.G. Ramos Sexually dimorphic expression of receptor-alpha in the cerebral cortex of neonatal Caiman latirostris (Crocodylia: Alligatoridae) Gen. Comp. Endocrinol. 179 2012 205 213
33. L. Monje, J. Varayoud, E.H. Luque, and J.G. Ramos Neonatal exposure to bisphenol A modifies the abundance of estrogen receptor alpha transcripts with alternative 5′-untranslated regions in the female rat preoptic area J. Endocrinol. 194 2007 201 212 (Pubitemid 47162899)
34. J.G. Ramos, J. Varayoud, L. Monje, G. Moreno-Piovano, M. Munoz-de-Toro, and E.H. Luque Diethylstilbestrol alters the population dynamic of neural precursor cells in the neonatal male rat dentate gyrus Brain Res. Bull. 71 2007 619 627 (Pubitemid 46209528)
35. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2005 Elsevier Academic Press Amsterdam
36. T.D. Palmer, A.R. Willhoite, and F.H. Gage Vascular niche for adult hippocampal neurogenesis J. Comp. Neurol. 425 2000 479 494
37. H.J. Gundersen, T.F. Bendtsen, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, and A. Vesterby et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis APMIS 96 1988 379 394
38. J.G. Herman, J.R. Graff, S. Myohanen, B.D. Nelkin, and S.B. Baylin Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands Proc. Natl. Acad. Sci. U. S. A. 93 1996 9821 9826 (Pubitemid 26296693)
39. J. Tost, and I.G. Gut DNA methylation analysis by pyrosequencing Nat. Protoc. 2 2007 2265 2275 (Pubitemid 351575045)
40. Z. Xiong, and P.W. Laird COBRA: a sensitive and quantitative DNA methylation assay Nucleic Acids Res. 25 1997 2532 2534 (Pubitemid 27303718)
41. J.M. Su, B. Yang, Y.S. Wang, Y.Y. Li, X.R. Xiong, L.J. Wang, Z.K. Guo, and Y. Zhang Expression and methylation status of imprinted genes in placentas of deceased and live cloned transgenic calves Theriogenology 75 2011 1346 1359
42. L.C. Li, and R. Dahiya MethPrimer: designing primers for methylation PCRs Bioinformatics 18 2002 1427 1431 (Pubitemid 35414532)
43. H. Thomassin, C. Kress, and T. Grange MethylQuant: a sensitive method for quantifying methylation of specific cytosines within the genome Nucleic Acids Res. 32 2004 e168
44. A.A. Walf, J.J. Paris, and C.A. Frye Chronic estradiol replacement to aged female rats reduces anxiety-like and depression-like behavior and enhances cognitive performance Psychoneuroendocrinology 34 2009 909 916
45. J.M. Daniel, and J. Bohacek The critical period hypothesis of estrogen effects on cognition: insights from basic research Biochim. Biophys. Acta 1800 2010 1068 1076
46. C.R. Clark, N.J. MacLusky, B. Parsons, and F. Naftolin Effects of estrogen deprivation on brain estrogen and progestin receptor levels and the activation of female sexual behavior Horm. Behav. 15 1981 289 298 (Pubitemid 11057747)
47. J.A. Czaja, and P.C. Butera Behavioral consequences of hormonal deprivation on the responsiveness of female rats to estradiol Physiol. Behav. 35 1985 873 877 (Pubitemid 16171264)
48. P.M. Maki, and V.W. Henderson Hormone therapy, dementia, and cognition: the Women's Health Initiative 10 years on Climacteric 15 2012 256 262
49. A.M. Barron, and C.J. Pike Sex hormones, aging, and Alzheimer's disease Front. Biosci. (Elite Ed.) 4 2012 976 997
50. M.M. Adams, T. Oung, J.H. Morrison, and A.C. Gore Length of postovariectomy interval and age, but not estrogen replacement, regulate N-methyl-d-aspartate receptor mRNA levels in the hippocampus of female rats Exp. Neurol. 170 2001 345 356 (Pubitemid 32758687)
51. R.T. Pereira, C.S. Porto, R.O. Godinho, and F.M. Abdalla Effects of estrogen on intracellular signaling pathways linked to activation of muscarinic acetylcholine receptors and on acetylcholinesterase activity in rat hippocampus Biochem. Pharmacol. 75 2008 1827 1834
52. H.E. Scharfman, and N.J. MacLusky Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS Front. Neuroendocrinol. 27 2006 415 435 (Pubitemid 44738017)
53. D.T. Solum, and R.J. Handa Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus J. Neurosci. 22 2002 2650 2659 (Pubitemid 37465814)
54. D.K. Binder, S.D. Croll, C.M. Gall, and H.E. Scharfman BDNF and epilepsy: too much of a good thing? Trends Neurosci. 24 2001 47 53 (Pubitemid 32332896)
55. J.M. Conner, J.C. Lauterborn, Q. Yan, C.M. Gall, and S. Varon Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport J. Neurosci. 17 1997 2295 2313 (Pubitemid 27137397)
56. Q.R. Liu, L. Lu, X.G. Zhu, J.P. Gong, Y. Shaham, and G.R. Uhl Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine Brain Res. 1067 2006 1 12 (Pubitemid 43133069)
57. T.L. Roth, and J.D. Sweatt Epigenetic marking of the BDNF gene by early-life adverse experiences Horm. Behav. 59 2011 315 320
58. M. Fagiolini, C.L. Jensen, and F.A. Champagne Epigenetic influences on brain development and plasticity Curr. Opin. Neurobiol. 19 2009 207 212
59. F. Gomez-Pinilla, Y. Zhuang, J. Feng, Z. Ying, and G. Fan Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation Eur. J. Neurosci. 33 2011 383 390
60. K.P. Guanaga, A. Kawano, and K.M. Menon In vivo effect of estradiol benzoate on the accumulation of adenosine 3′,5′-cyclic monophosphate in the rat hypothalamus Neuroendocrinology 16 1974 273 281
61. J.J. Watters, and D.M. Dorsa Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms J. Neurosci. 18 1998 6672 6680 (Pubitemid 28387999)
62. P.S. Green, and J.W. Simpkins Neuroprotective effects of estrogens: potential mechanisms of action Int. J. Dev. Neurosci. 18 2000 347 358 (Pubitemid 30243066)
63. K. Singh, and S. Prasad Age- and sex-related analysis of methylation of 5′-upstream sequences of Fmr-1 gene in mouse brain and modulation by sex steroid hormones Biogerontology 9 2008 455 465
64. M. Blurton-Jones, P.N. Kuan, and M.H. Tuszynski Anatomical evidence for transsynaptic influences of estrogen on brain-derived neurotrophic factor expression J. Comp. Neurol. 468 2004 347 360 (Pubitemid 37549655)
65. S.A. Hart, J.D. Patton, and C.S. Woolley Quantitative analysis of ER alpha and GAD colocalization in the hippocampus of the adult female rat J. Comp. Neurol. 440 2001 144 155 (Pubitemid 33032442)
66. C.S. Woolley Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus Horm. Behav. 34 1998 140 148 (Pubitemid 28541755)
67. E. Castren, B. Berninger, A. Leingartner, and D. Lindholm Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity Prog. Brain Res. 117 1998 57 64 (Pubitemid 28530681)
68. C.I. Sze, H. Bi, B.K. Kleinschmidt-DeMasters, C.M. Filley, and L.J. Martin Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer's disease brains J. Neurol. Sci. 175 2000 81 90 (Pubitemid 30265473)
69. T. Bittner, M. Fuhrmann, S. Burgold, S.M. Ochs, N. Hoffmann, G. Mitteregger, H. Kretzschmar, F.M. LaFerla, and J. Herms Multiple events lead to dendritic spine loss in triple transgenic Alzheimer's disease mice PLoS One 5 2010 e15477
70. M. Pan, Z. Li, V. Yeung, and R.J. Xu Dietary supplementation of soy germ phytoestrogens or estradiol improves spatial memory performance and increases gene expression of BDNF TrkB receptor and synaptic factors in ovariectomized rats Nutr. Metab. (Lond.) 7 2010 75
71. J.L. Spencer, E.M. Waters, T.A. Milner, and B.S. McEwen Estrous cycle regulates activation of hippocampal Akt LIM kinase, and neurotrophin receptors in C57BL/6 mice Neuroscience 155 2008 1106 1119 Técnicas