Epigenetic setting for long-term expression of estrogen receptor α and androgen receptor in cells

Hormones and Behavior

Volumn 59, Issue 3, 2011, Pages 345-352

  Imamura, Takuya ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Androgen receptor; Autoregulation; Brain masculinization; Cell memory; DNA methylation; Estrogen receptor

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ESTROGEN; ESTROGEN RECEPTOR ALPHA; GENOMIC DNA; ISOPROTEIN; TESTOSTERONE;

ANDROGEN RESPONSIVE ELEMENT; AUTOREGULATION; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN MASCULINIZATION; CANCER CELL; CHROMOSOME; DNA METHYLATION; DNA STRUCTURE; EPIGENETICS; ESTROGEN RESPONSIVE ELEMENT; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; MAMMAL; NONHUMAN; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; SEX DIFFERENTIATION; VERTEBRATE;

ANIMALS; BRAIN; DNA METHYLATION; EPIGENESIS, GENETIC; ESTROGEN RECEPTOR ALPHA; HOMEOSTASIS; NEURONS; RECEPTORS, ANDROGEN; SEX DIFFERENTIATION;

EID: 79952697168     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.05.018     Document Type: Review

References (103)

1. Agarwal V.R., Sinton C.M., Liang C., Fisher C., German D.C., Simpson E.R. Upregulation of estrogen receptors in the forebrain of aromatase knockout (ArKO) mice. Mol. Cell. Endocrinol. 2000, 162:9-16.
2. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23:185-188.
3. Antonio J., Wilson J.D., George F.W. Effects of castration and androgen treatment on androgen-receptor levels in rat skeletal muscles. J. Appl. Physiol. 1999, 87:2016-2019.
4. Arai Y., Murakami S., Nishizuka M. Androgen enhances neuronal degeneration in the developing preoptic area: apoptosis in the anteroventral periventricular nucleus (AVPvN-POA). Horm. Behav. 1994, 28:313-319.
5. Arai Y., Sekine Y., Murakami S. Estrogen and apoptosis in the developing sexually dimorphic preoptic area in female rats. Neurosci. Res. 1996, 25:403-407.
6. Bajic V.B., Tan S.L., Chong A., Tang S., Strom A., Gustafsson J.A., Lin C.Y., Liu E.T. Dragon ERE Finder version 2: a tool for accurate detection and analysis of estrogen response elements in vertebrate genomes. Nucleic Acids Res. 2003, 31:3605-3607.
7. Baum M.J. Effects of testosterone propionate administered perinatally on sexual behavior of female ferrets. J. Comp. Physiol. Psychol. 1976, 90:399-410.
8. Baum M.J. A comparison of the effects of methyltrienolone (R 1881) and 5 alpha-dihydrotestosterone on sexual behavior of castrated male rats. Horm. Behav. 1979, 13:165-174.
9. Baum M.J., Gallagher C.A., Martin J.T., Damassa D.A. Effects of testosterone, dihydrotestosterone, or estradiol administered neonatally on sexual behavior of female ferrets. Endocrinology 1982, 111:773-780.
10. Baum M.J., Canick J.A., Erskine M.S., Gallagher C.A., Shim J.H. Normal differentiation of masculine sexual behavior in male ferrets despite neonatal inhibition of brain aromatase or 5-alpha-reductase activity. Neuroendocrinology 1983, 36:277-284.
11. Baylin S.B., Herman J.G., Graff J.R., Vertino P.M., Issa J.P. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 1998, 72:141-196.
12. Bird A.P., Wolffe A.P. Methylation-induced repression-belts, braces, and chromatin. Cell 1999, 99:451-454.
13. Bourdeau V., Deschenes J., Metivier R., Nagai Y., Nguyen D., Bretschneider N., Gannon F., White J.H., Mader S. Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol. Endocrinol. 2004, 18:1411-1427.
14. Bronson F.H. The regulation of luteinizing hormone secretion by estrogen: relationships among negative feedback, surge potential, and male stimulation in juvenile, peripubertal, and adult female mice. Endocrinology 1981, 108:506-516.
15. Christian C.A., Mobley J.L., Moenter S.M. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15682-15687.
16. Chung W.C., Swaab D.F., De Vries G.J. Apoptosis during sexual differentiation of the bed nucleus of the stria terminalis in the rat brain. J. Neurobiol. 2000, 43:234-243.
17. Clancy A.N., Michael R.P. Effects of testosterone and aromatase inhibition on estrogen receptor-like immunoreactivity in male rat brain. Neuroendocrinology 1994, 59:552-560.
18. Collas P. Modulation of plasmid DNA methylation and expression in zebrafish embryos. Nucleic Acids Res. 1998, 26:4454-4461.
19. Cooke B., Hegstrom C.D., Villeneuve L.S., Breedlove S.M. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 1998, 19:323-362.
20. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
21. Cross S., Kovarik P., Schmidtke J., Bird A. Non-methylated islands in fish genomes are GC-poor. Nucleic Acids Res. 1991, 19:1469-1474.
22. Donaghue C., Westley B.R., May F.E. Selective promoter usage of the human estrogen receptor-alpha gene and its regulation by estrogen. Mol. Endocrinol. 1999, 13:1934-1950.
23. DonCarlos L.L., Malik K., Morrell J.I. Region-specific effects of ovarian hormones on estrogen receptor immunoreactivity. Neuroreport 1995, 6:2054-2058.
24. Eden A., Gaudet F., Waghmare A., Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003, 300:455.
25. Feder H.H., Naftolin F., Ryan K.J. Male and female sexual responses in male rats given estradiol benzoate and 5 alpha-androstan-17 beta-ol-3-one propionate. Endocrinology 1974, 94:136-141.
26. Ferguson A.T., Lapidus R.G., Baylin S.B., Davidson N.E. Demethylation of the estrogen receptor gene in estrogen receptor-negative breast cancer cells can reactivate estrogen receptor gene expression. Cancer Res. 1995, 55:2279-2283.
27. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
28. Fremont M., Siegmann M., Gaulis S., Matthies R., Hess D., Jost J.P. Demethylation of DNA by purified chick embryo 5-methylcytosine-DNA glycosylase requires both protein and RNA. Nucleic Acids Res. 1997, 25:2375-2380.
29. Fullwood M.J., Liu M.H., Pan Y.F., Liu J., Xu H., Mohamed Y.B., Orlov Y.L., Velkov S., Ho A., Mei P.H., Chew E.G., Huang P.Y., Welboren W.J., Han Y., Ooi H.S., Ariyaratne P.N., Vega V.B., Luo Y., Tan P.Y., Choy P.Y., Wansa K.D., Zhao B., Lim K.S., Leow S.C., Yow J.S., Joseph R., Li H., Desai K.V., Thomsen J.S., Lee Y.K., Karuturi R.K., Herve T., Bourque G., Stunnenberg H.G., Ruan X., Cacheux-Rataboul V., Sung W.K., Liu E.T., Wei C.L., Cheung E., Ruan Y. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009, 462:58-64.
30. Funakoshi T., Yanai A., Shinoda K., Kawano M.M., Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem. Biophys. Res. Commun. 2006, 346:904-910.
31. Gonzalez-Cadavid N., Vernet D., Fuentes Navarro A., Rodriguez J.A., Swerdloff R.S., Rajfer J. Up-regulation of the levels of androgen receptor and its mRNA by androgens in smooth-muscle cells from rat penis. Mol. Cell. Endocrinol. 1993, 90:219-229.
32. Goodman R.L. A quantitative analysis of the physiological role of estradiol and progesterone in the control of tonic and surge secretion of luteinizing hormone in the rat. Endocrinology 1978, 102:142-150.
33. Grober M.S., Sunobe T. Serial adult sex change involves rapid and reversible changes in forebrain neurochemistry. Neuroreport 1996, 7:2945-2949.
34. Gruber C.J., Gruber D.M., Gruber I.M., Wieser F., Huber J.C. Anatomy of the estrogen response element. Trends Endocrinol. Metab. 2004, 15:73-78.
35. Hackenberg R., Hawighorst T., Filmer A., Slater E.P., Bock K., Beato M., Schulz K.D. Regulation of androgen receptor mRNA and protein level by steroid hormones in human mammary cancer cells. J. Steroid Biochem. Mol. Biol. 1992, 43:599-607.
36. Hamada T., Wada-Kiyama Y., Sakuma Y. Visualizing forebrain-specific usage of an estrogen receptor alpha promoter for receptor downregulation in the rat. Brain Res. Mol. Brain Res. 2005, 139:42-51.
37. Handa R.J., Kerr J.E., DonCarlos L.L., McGivern R.F., Hejna G. Hormonal regulation of androgen receptor messenger RNA in the medial preoptic area of the male rat. Brain Res. Mol. Brain Res. 1996, 39:57-67.
38. Hansen R.S., Wijmenga C., Luo P., Stanek A.M., Canfield T.K., Weemaes C.M., Gartler S.M. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:14412-14417.
39. Heard E., Mongelard F., Arnaud D., Avner P. Xist yeast artificial chromosome transgenes function as X-inactivation centers only in multicopy arrays and not as single copies. Mol. Cell. Biol. 1999, 19:3156-3166.
40. Heinzel T., Lavinsky R.M., Mullen T.M., Soderstrom M., Laherty C.D., Torchia J., Yang W.M., Brard G., Ngo S.D., Davie J.R., Seto E., Eisenman R.N., Rose D.W., Glass C.K., Rosenfeld M.G. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 1997, 387:43-48.
41. Hsu H.K., Yang R.C., Shih H.C., Hsieh Y.L., Chen U.Y., Hsu C. Prenatal exposure of testosterone prevents SDN-POA neurons of postnatal male rats from apoptosis through NMDA receptor. J. Neurophysiol. 2001, 86:2374-2380.
42. Imamura T., Ohgane J., Ito S., Ogawa T., Hattori N., Tanaka S., Shiota K. CpG island of rat sphingosine kinase-1 gene: tissue-dependent DNA methylation status and multiple alternative first exons. Genomics 2001, 76:117-125.
43. Imamura T., Yamamoto S., Ohgane J., Hattori N., Tanaka S., Shiota K. Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem. Biophys. Res. Commun. 2004, 322:593-600.
44. Ing N.H., Tornesi M.B. Estradiol up-regulates estrogen receptor and progesterone receptor gene expression in specific ovine uterine cells. Biol. Reprod. 1997, 56:1205-1215.
45. Jarrard D.F., Kinoshita H., Shi Y., Sandefur C., Hoff D., Meisner L.F., Chang C., Herman J.G., Isaacs W.B., Nassif N. Methylation of the androgen receptor promoter CpG island is associated with loss of androgen receptor expression in prostate cancer cells. Cancer Res. 1998, 58:5310-5314.
46. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
47. Jones P.A., Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001, 293:1068-1070.
48. Jost J.P., Jost Y.C. Transient DNA demethylation in differentiating mouse myoblasts correlates with higher activity of 5-methyldeoxycytidine excision repair. J. Biol. Chem. 1994, 269:10040-10043.
49. Jost J.P., Siegmann M., Sun L., Leung R. Mechanisms of DNA demethylation in chicken embryos. Purification and properties of a 5-methylcytosine-DNA glycosylase. J. Biol. Chem. 1995, 270:9734-9739.
50. Jost J.P., Fremont M., Siegmann M., Hofsteenge J. The RNA moiety of chick embryo 5-methylcytosine-DNA glycosylase targets DNA demethylation. Nucleic Acids Res. 1997, 25:4545-4550.
51. Jost J.P., Siegmann M., Thiry S., Jost Y.C., Benjamin D., Schwarz S. A re-investigation of the ribonuclease sensitivity of a DNA demethylation reaction in chicken embryo and G8 mouse myoblasts. FEBS Lett. 1999, 449:251-254.
52. Kaneko K.J., Furlow J.D., Gorski J. Involvement of the coding sequence for the estrogen receptor gene in autologous ligand-dependent down-regulation. Mol. Endocrinol. 1993, 7:879-888.
53. Kerr J.E., Allore R.J., Beck S.G., Handa R.J. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 1995, 136:3213-3221.
54. Khetawat G., Faraday N., Nealen M.L., Vijayan K.V., Bolton E., Noga S.J., Bray P.F. Human megakaryocytes and platelets contain the estrogen receptor beta and androgen receptor (AR): testosterone regulates AR expression. Blood 2000, 95:2289-2296.
55. Kim M.S., Kondo T., Takada I., Youn M.Y., Yamamoto Y., Takahashi S., Matsumoto T., Fujiyama S., Shirode Y., Yamaoka I., Kitagawa H., Takeyama K., Shibuya H., Ohtake F., Kato S. DNA demethylation in hormone-induced transcriptional derepression. Nature 2009, 461:1007-1012.
56. Kinoshita H., Shi Y., Sandefur C., Meisner L.F., Chang C., Choon A., Reznikoff C.R., Bova G.S., Friedl A., Jarrard D.F. Methylation of the androgen receptor minimal promoter silences transcription in human prostate cancer. Cancer Res. 2000, 60:3623-3630.
57. Klein-Hitpass L., Schorpp M., Wagner U., Ryffel G.U. An estrogen-responsive element derived from the 5' flanking region of the Xenopus vitellogenin A2 gene functions in transfected human cells. Cell 1986, 46:1053-1061.
58. Kos M., Reid G., Denger S., Gannon F. Minireview: genomic organization of the human ERalpha gene promoter region. Mol. Endocrinol. 2001, 15:2057-2063.
59. Kovalchuk O., Tryndyak V.P., Montgomery B., Boyko A., Kutanzi K., Zemp F., Warbritton A.R., Latendresse J.R., Kovalchuk I., Beland F.A., Pogribny I.P. Estrogen-induced rat breast carcinogenesis is characterized by alterations in DNA methylation, histone modifications and aberrant microRNA expression. Cell Cycle 2007, 6:2010-2018.
60. Kraeling R.R., Johnson B., Barb C.R., Rampacek G.B. Evidence for a luteinizing hormone surge center in the hypothalamus of the pig. Biol. Reprod. 1998, 58:1199-1205.
61. Krongrad A., Wilson C.M., Wilson J.D., Allman D.R., McPhaul M.J. Androgen increases androgen receptor protein while decreasing receptor mRNA in LNCaP cells. Mol. Cell. Endocrinol. 1991, 76:79-88.
62. Kumar R.C., Thakur M.K. Androgen receptor mRNA is inversely regulated by testosterone and estradiol in adult mouse brain. Neurobiol. Aging 2004, 25:925-933.
63. Kumar R.C., Thakur M.K. Sex steroids reduce DNaseI accessibility of androgen receptor promoter in adult male mice brain. Brain Res. Mol. Brain Res. 2004, 131:1-7.
64. Kunert N., Marhold J., Stanke J., Stach D., Lyko F. A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 2003, 130:5083-5090.
65. Lauber A.H., Mobbs C.V., Muramatsu M., Pfaff D.W. Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 1991, 129:3180-3186.
66. Leu Y.W., Yan P.S., Fan M., Jin V.X., Liu J.C., Curran E.M., Welshons W.V., Wei S.H., Davuluri R.V., Plass C., Nephew K.P., Huang T.H. Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res. 2004, 64:8184-8192.
67. Lindzey J., Wetsel W.C., Couse J.F., Stoker T., Cooper R., Korach K.S. Effects of castration and chronic steroid treatments on hypothalamic gonadotropin-releasing hormone content and pituitary gonadotropins in male wild-type and estrogen receptor-alpha knockout mice. Endocrinology 1998, 139:4092-4101.
68. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
69. Lyko F., Ramsahoye B.H., Jaenisch R. DNA methylation in Drosophila melanogaster. Nature 2000, 408:538-540.
70. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., Flavell R.A., Lu B., Ming G.L., Song H. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009, 323:1074-1077.
71. McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
72. McCarthy M.S., Swanson L.V. Serum LH concentration following castration, steroid hormone and gonadotropin releasing hormone treatment in the male bovine. J. Anim. Sci. 1976, 43:151-158.
73. Morali G., Larsson K., Beyer C. Inhibition of testosterone-induced sexual behavior in the castrated male rat by aromatase blockers. Horm. Behav. 1977, 9:203-213.
74. Mori Y., Tanaka M., Maeda K., Hoshino K., Kano Y. Photoperiodic modification of negative and positive feedback effects of oestradiol on LH secretion in ovariectomized goats. J. Reprod. Fertil. 1987, 80:523-529.
75. Nastiuk K.L., Clayton D.F. Seasonal and tissue-specific regulation of canary androgen receptor messenger ribonucleic acid. Endocrinology 1994, 134:640-649.
76. Ohgane J., Hattori N., Oda M., Tanaka S., Shiota K. Differentiation of trophoblast lineage is associated with DNA methylation and demethylation. Biochem. Biophys. Res. Commun. 2002, 290:701-706.
77. Ottaviano Y.L., Issa J.P., Parl F.F., Smith H.S., Baylin S.B., Davidson N.E. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res. 1994, 54:2552-2555.
78. Pink J.J., Jordan V.C. Models of estrogen receptor regulation by estrogens and antiestrogens in breast cancer cell lines. Cancer Res. 1996, 56:2321-2330.
79. Pomerantz S.M., Goy R.W., Roy M.M. Expression of male-typical behavior in adult female pseudohermaphroditic rhesus: comparisons with normal males and neonatally gonadectomized males and females. Horm. Behav. 1986, 20:483-500.
80. Putnam S.K., Sato S., Hull E.M. Effects of testosterone metabolites on copulation and medial preoptic dopamine release in castrated male rats. Horm. Behav. 2003, 44:419-426.
81. Qiu J., Bosch M.A., Tobias S.C., Grandy D.K., Scanlan T.S., Ronnekleiv O.K., Kelly M.J. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 2003, 23:9529-9540.
82. Qiu J., Bosch M.A., Tobias S.C., Krust A., Graham S.M., Murphy S.J., Korach K.S., Chambon P., Scanlan T.S., Ronnekleiv O.K., Kelly M.J. A G-protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J. Neurosci. 2006, 26:5649-5655.
83. Quarmby V.E., Yarbrough W.G., Lubahn D.B., French F.S., Wilson E.M. Autologous down-regulation of androgen receptor messenger ribonucleic acid. Mol. Endocrinol. 1990, 4:22-28.
84. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005, 307:1625-1630.
85. Saceda M., Lippman M.E., Chambon P., Lindsey R.L., Ponglikitmongkol M., Puente M., Martin M.B. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol. 1988, 2:1157-1162.
86. Sato T., Matsumoto T., Kawano H., Watanabe T., Uematsu Y., Sekine K., Fukuda T., Aihara K., Krust A., Yamada T., Nakamichi Y., Yamamoto Y., Nakamura T., Yoshimura K., Yoshizawa T., Metzger D., Chambon P., Kato S. Brain masculinization requires androgen receptor function. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1673-1678.
87. Schwarz J.M., McCarthy M.M. Cellular mechanisms of estradiol-mediated masculinization of the brain. J. Steroid Biochem. Mol. Biol. 2008, 109:300-306.
88. Seale J.V., Wood S.A., Atkinson H.C., Harbuz M.S., Lightman S.L. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 2004, 16:989-998.
89. Shan L.X., Rodriguez M.C., Janne O.A. Regulation of androgen receptor protein and mRNA concentrations by androgens in rat ventral prostate and seminal vesicles and in human hepatoma cells. Mol. Endocrinol. 1990, 4:1636-1646.
90. Sharif J., Muto M., Takebayashi S., Suetake I., Iwamatsu A., Endo T.A., Shinga J., Mizutani-Koseki Y., Toyoda T., Okamura K., Tajima S., Mitsuya K., Okano M., Koseki H. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
91. Shiota K., Yanagimachi R. Epigenetics by DNA methylation for development of normal and cloned animals. Differentiation 2002, 69:162-166.
92. Shiota K., Kogo Y., Ohgane J., Imamura T., Urano A., Nishino K., Tanaka S., Hattori N. Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 2002, 7:961-969.
93. Shughrue P.J., Bushnell C.D., Dorsa D.M. Estrogen receptor messenger ribonucleic acid in female rat brain during the estrous cycle: a comparison with ovariectomized females and intact males. Endocrinology 1992, 131:381-388.
94. Sodersten P. Effects of anti-oestrogen treatment of neonatal male rats on lordosis behaviour and mounting behaviour in the adult. J. Endocrinol. 1978, 76:241-249.
95. Toran-Allerand C.D. Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann. N. Y. Acad. Sci. 2005, 1052:136-144.
96. Walsh C.P., Bestor T.H. Cytosine methylation and mammalian development. Genes Dev. 1999, 13:26-34.
97. Webb R., England B.G., Fitzpatrick K.E. Control of the preovulatory gonadotropin surge in the ewe. Endocrinology 1981, 108:1178-1185.
98. Westberry J.M., Trout A.L., Wilson M.E. Epigenetic regulation of estrogen receptor alpha gene expression in the mouse cortex during early postnatal development. Endocrinology 2010, 151:731-740.
99. Wilson M.E., Westberry J.M., Prewitt A.K. Dynamic regulation of estrogen receptor-alpha gene expression in the brain: a role for promoter methylation?. Front. Neuroendocrinol. 2008, 29:375-385.
100. Wiren K.M., Zhang X., Chang C., Keenan E., Orwoll E.S. Transcriptional up-regulation of the human androgen receptor by androgen in bone cells. Endocrinology 1997, 138:2291-2300.
101. Wolf D.A., Herzinger T., Hermeking H., Blaschke D., Horz W. Transcriptional and posttranscriptional regulation of human androgen receptor expression by androgen. Mol. Endocrinol. 1993, 7:924-936.
102. Xu G.L., Bestor T.H., Bourc'his D., Hsieh C.L., Tommerup N., Bugge M., Hulten M., Qu X., Russo J.J., Viegas-Pequignot E. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 1999, 402:187-191.
103. Yang X., Ferguson A.T., Nass S.J., Phillips D.L., Butash K.A., Wang S.M., Herman J.G., Davidson N.E. Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition. Cancer Res. 2000, 60:6890-6894.