Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action

Steroids

Volumn 75, Issue 7, 2010, Pages 467-476

  Martinez Arguelles, Daniel B ^a,b,c   Papadopoulos, Vassilios ^a,b,c  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

DNA methylation; Epigenetics; Nuclear receptors; Steroid hormones; Steroidogenesis; Transcription factors

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANDROGEN RECEPTOR; AROMATASE; AZACITIDINE; CELL NUCLEUS RECEPTOR; CYTIDINE; CYTOCHROME P450 17; CYTOCHROME P450 17A1; ESTROGEN RECEPTOR; GLUCOCORTICOID RECEPTOR; HISTONE; HISTONE DEACETYLASE INHIBITOR; MINERALOCORTICOID RECEPTOR; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROIDOGENIC FACTOR 1; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID;

ACETYLATION; CLINICAL TRIAL; CPG ISLAND; DNA METHYLATION; DRUG MECHANISM; ENZYME REGULATION; EPIGENETICS; EPILEPSY; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; HORMONE ACTION; HUMAN; IN VIVO STUDY; NONHUMAN; PHYSIOLOGICAL PROCESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; REVIEW; SIDE EFFECT; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; BIOSYNTHETIC PATHWAYS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; PHOSPHOPROTEINS; STEROID 17-ALPHA-HYDROXYLASE; STEROIDOGENIC FACTOR 1; STEROIDS;

EID: 77951108967     PISSN: 0039128X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.steroids.2010.02.004     Document Type: Review

References (137)

1. Barros S.P., and Offenbacher S. Epigenetics: connecting environment and genotype to phenotype and disease. J Dent Res 88 (2009) 400-408
2. Meaney M.J., and Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci 7 (2005) 103-123
3. Simmons R.A. Developmental origins of adult disease. Pediatr Clin North Am 56 (2009) 449-466
4. Baulieu E.E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 23 (1998) 963-987
5. Mellon S.H., and Griffin L.D. Neurosteroids: biochemistry and clinical significance. Trends Endocrinol Metab 13 (2002) 35-43
6. Brown R.C., Cascio C., and Papadopoulos V. Pathways of neurosteroid biosynthesis in cell lines from human brain: regulation of dehydroepiandrosterone formation by oxidative stress and beta-amyloid peptide. J Neurochem 74 (2000) 847-859
7. Kayes-Wandover K.M., and White P.C. Steroidogenic enzyme gene expression in the human heart. J Clin Endocrinol Metab 85 (2000) 2519-2525
8. Young M.J., Clyne C.D., Cole T.J., and Funder J.W. Cardiac steroidogenesis in the normal and failing heart. J Clin Endocrinol Metab 86 (2001) 5121-5126
9. White P.C. Aldosterone: direct effects on and production by the heart. J Clin Endocrinol Metab 88 (2003) 2376-2383
10. Jefcoate C.R. Liver X receptor opens a new gateway to StAR and to steroid hormones. J Clin Invest 116 (2006) 1832-1835
11. Rone M.B., Fan J., and Papadopoulos V. Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim Biophys Acta 1791 (2009) 646-658
12. Brock B.J., and Waterman M.R. Biochemical differences between rat and human cytochrome P450c17 support the different steroidogenic needs of these two species. Biochemistry 38 (1999) 1598-1606
13. Pelletier G., Li S., Luu-The V., Tremblay Y., Belanger A., and Labrie F. Immunoelectron microscopic localization of three key steroidogenic enzymes (cytochrome P450(scc), 3 beta-hydroxysteroid dehydrogenase and cytochrome P450(c17)) in rat adrenal cortex and gonads. J Endocrinol 171 (2001) 373-383
14. Perkins L.M., and Payne A.H. Quantification of P450scc, P450(17) alpha, and iron sulfur protein reductase in Leydig cells and adrenals of inbred strains of mice. Endocrinology 123 (1988) 2675-2682
15. Lavoie H.A., and King S.R. Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B. Exp Biol Med (Maywood) 234 (2009) 880-907
16. Brinkmann A.O. Molecular basis of androgen insensitivity. Mol Cell Endocrinol 179 (2001) 105-109
17. Zhang J., Ge R., Matte-Martone C., Goodwin J., Shlomchik W.D., Mamula M.J., et al. Characterization of a novel gain of function glucocorticoid receptor knock-in mouse. J Biol Chem 284 (2009) 6249-6259
18. Miller W.L. Steroidogenic enzymes. Endocr Dev 13 (2008) 1-18
19. Payne A.H., and Hales D.B. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25 (2004) 947-970
20. Bird A.P. CpG-rich islands and the function of DNA methylation. Nature 321 (1986) 209-213
21. Han L., and Zhao Z. CpG islands or CpG clusters: how to identify functional GC-rich regions in a genome?. BMC Bioinform 10 (2009) 65
22. Prokhorchuk A.V., Aitkhozhina D.S., Sablina A.A., Ruzov A.S., and Prokhorchuk E.B. KAISO-a new member of the BTB/POZ family specifically bindsto methylated DNA sequences. Genetika 37 (2001) 737-744
23. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19 (1998) 187-191
24. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393 (1998) 386-389
25. Watt F., and Molloy P.L. Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 2 (1988) 1136-1143
26. Tate P.H., and Bird A.P. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr Opin Genet Dev 3 (1993) 226-231
27. Okano M., Xie S., and Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19 (1998) 219-220
28. Li E., Bestor T.H., and Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69 (1992) 915-926
29. Goll M.G., Kirpekar F., Maggert K.A., Yoder J.A., Hsieh C.L., Zhang X., et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311 (2006) 395-398
30. Jeltsch A., Nellen W., and Lyko F. Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 31 (2006) 306-308
31. Okano M., Bell D.W., Haber D.A., and Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99 (1999) 247-257
32. Hata K., Okano M., Lei H., and Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129 (2002) 1983-1993
33. Kaneda M., Okano M., Hata K., Sado T., Tsujimoto N., Li E., et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429 (2004) 900-903
34. Zhang Y., and Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15 (2001) 2343-2360
35. Henikoff S., and Ahmad K. Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 21 (2005) 133-153
36. Wade P.A., Pruss D., and Wolffe A.P. Histone acetylation: chromatin in action. Trends Biochem Sci 22 (1997) 128-132
37. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol 11 (2001) 266-273
38. Shiio Y., and Eisenman R.N. Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100 (2003) 13225-13230
39. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75 (2006) 243-269
40. Tamaru H., Zhang X., McMillen D., Singh P.B., Nakayama J., Grewal S.I., et al. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34 (2003) 75-79
41. Bolden J.E., Peart M.J., and Johnstone R.W. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5 (2006) 769-784
42. Chen W.Y., Bailey E.C., McCune S.L., Dong J.Y., and Townes T.M. Reactivation of silenced, virally transduced genes by inhibitors of histone deacetylase. Proc Natl Acad Sci USA 94 (1997) 5798-5803
43. Gregoraszczuk E., Wojtowicz A.K., Tauboll E., and Ropstad E. Valproate-induced alterations in testosterone, estradiol and progesterone secretion from porcine follicular cells isolated from small- and medium-sized ovarian follicles. Seizure 9 (2000) 480-485
44. Mikkonen K., Vainionpaa L.K., Pakarinen A.J., Knip M., Jarvela I.Y., Tapanainen J.S., et al. Long-term reproductive endocrine health in young women with epilepsy during puberty. Neurology 62 (2004) 445-450
45. Hatano O., Takakusu A., Nomura M., and Morohashi K. Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1 (1996) 663-671
46. Bamberger A.M., Ezzat S., Cao B., Wong M., Parker K.L., Schulte H.M., et al. Expression of steroidogenic factor-1 (SF-1) mRNA and protein in the human placenta. Mol Hum Reprod 2 (1996) 457-461
47. Morohashi K., Honda S., Inomata Y., Handa H., and Omura T. A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem 267 (1992) 17913-17919
48. Parker K.L., Rice D.A., Lala D.S., Ikeda Y., Luo X., Wong M., et al. Steroidogenic factor 1: an essential mediator of endocrine development. Recent Prog Horm Res 57 (2002) 19-36
49. Sugawara T., Sakuragi N., and Minakami H. CREM confers cAMP responsiveness in human steroidogenic acute regulatory protein expression in NCI-H295R cells rather than SF-1/Ad4BP. J Endocrinol 191 (2006) 327-337
50. Lin L., and Achermann J.C. Steroidogenic factor-1 (SF-1, Ad4BP, NR5A1) and disorders of testis development. Sex Dev 2 (2008) 200-209
51. Xue Q., Lin Z., Yin P., Milad M.P., Cheng Y.H., Confino E., et al. Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5′ CpG island in endometriosis. J Clin Endocrinol Metab 92 (2007) 3261-3267
52. Chen W.Y., Weng J.H., Huang C.C., and Chung B.C. Histone deacetylase inhibitors reduce steroidogenesis through SCF-mediated ubiquitination and degradation of steroidogenic factor 1 (NR5A1). Mol Cell Biol 27 (2007) 7284-7290
53. Hiroi H., Christenson L.K., and Strauss III J.F. Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Mol Cell Endocrinol 215 (2004) 119-126
54. Hiroi H., Christenson L.K., Chang L., Sammel M.D., Berger S.L., and Strauss III J.F. Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (stAR) locus associated with stAR transcription. Mol Endocrinol 18 (2004) 791-806
55. Missaghian E., Kempna P., Dick B., Hirsch A., Ikhani-Koupaei R., Jegou B., et al. Role of DNA methylation in the tissue-specific expression of the CYP17A1 gene for steroidogenesis in rodents. J Endocrinol 202 (2009) 99-109
56. Chung B.C., Picado-Leonard J., Haniu M., Bienkowski M., Hall P.F., Shively J.E., et al. Cytochrome P450c17 (steroid 17 alpha-hydroxylase/17,20 lyase): cloning of human adrenal and testis cDNAs indicates the same gene is expressed in both tissues. Proc Natl Acad Sci USA 84 (1987) 407-411
57. Johnson D.C., and Sen M. The cytochrome P450(17) alpha (17 alpha-hydroxylase/C17,20-lyase) activity of the junctional zone of the rat placenta. J Endocrinol 125 (1990) 217-224
58. Namiki M., Kitamura M., Buczko E., and Dufau M.L. Rat testis P-450(17)alpha cDNA: the deduced amino acid sequence, expression and secondary structural configuration. Biochem Biophys Res Commun 157 (1988) 705-712
59. Hornsby P.J., Yang L.Q., Raju S.G., and Cheng C.Y. Changes in gene expression and DNA methylation in adrenocortical cells senescing in culture. Mutat Res 256 (1991) 105-113
60. Hornsby P.J., Yang L., Raju S.G., Maghsoudlou S.S., Lala D.S., and Nallaseth F.S. Demethylation of specific sites in the 5′-flanking region of the CYP17 genes when bovine adrenocortical cells are placed in culture. DNA Cell Biol 11 (1992) 385-395
61. Sewer M.B., and Jagarlapudi S. Complex assembly on the human CYP17 promoter. Mol Cell Endocrinol 300 (2009) 109-114
62. Fluck C.E., and Miller W.L. GATA-4 and GATA-6 modulate tissue-specific transcription of the human gene for P450c17 by direct interaction with Sp1. Mol Endocrinol 18 (2004) 1144-1157
63. Chen D., Reierstad S., Lu M., Lin Z., Ishikawa H., and Bulun S.E. Regulation of breast cancer-associated aromatase promoters. Cancer Lett 273 (2009) 15-27
64. Vanselow J., Pohland R., and Furbass R. Promoter-2-derived Cyp19 expression in bovine granulosa cells coincides with gene-specific DNA hypo-methylation. Mol Cell Endocrinol 233 (2005) 57-64
65. Demura M., and Bulun S.E. CpG dinucleotide methylation of the CYP19 I.3/II promoter modulates cAMP-stimulated aromatase activity. Mol Cell Endocrinol 283 (2008) 127-132
66. Zhou J., Gurates B., Yang S., Sebastian S., and Bulun S.E. Malignant breast epithelial cells stimulate aromatase expression via promoter II in human adipose fibroblasts: an epithelial-stromal interaction in breast tumors mediated by CCAAT/enhancer binding protein beta. Cancer Res 61 (2001) 2328-2334
67. Zhou D., and Chen S. Identification and characterization of a cAMP-responsive element in the region upstream from promoter 1.3 of the human aromatase gene. Arch Biochem Biophys 371 (1999) 179-190
68. Furbass R., Selimyan R., and Vanselow J. DNA methylation and chromatin accessibility of the proximal Cyp 19 promoter region 1.5/2 correlate with expression levels in sheep placentomes. Mol Reprod Dev 75 (2008) 1-7
69. Vanselow J., Selimyan R., and Furbass R. DNA methylation of placenta-specific Cyp19 promoters of cattle and sheep. Exp Clin Endocrinol Diabetes 116 (2008) 437-442
70. Tsai M.J., and O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63 (1994) 451-486
71. Robinson-Rechavi M., Escriva G.H., and Laudet V. The nuclear receptor superfamily. J Cell Sci 116 (2003) 585-586
72. Gottlieb B., Beitel L.K., Wu J., Elhaji Y.A., and Trifiro M. Nuclear receptors and disease: androgen receptor. Essays Biochem 40 (2004) 121-136
73. Komesaroff P.A., Funder J.W., and Fuller P.J. Hormone-nuclear receptor interactions in health and disease. Mineralocorticoid resistance. Baillieres Clin Endocrinol Metab 8 (1994) 333-355
74. Meyers C.Y., Hou Y., Winters T.A., Banz W.J., and Adler S. Activities of a non-classical estrogen, Z-bis-dehydrodoisynolic acid, with ERalpha and ERbeta. J Steroid Biochem Mol Biol 82 (2002) 33-44
75. 18F]fluorodoisynolic acids. Nucl Med Biol 24 (1997) 209-224
76. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
77. Francis D., Diorio J., Liu D., and Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286 (1999) 1155-1158
78. Kolber B.J., Wieczorek L., and Muglia L.J. Hypothalamic-pituitary-adrenal axis dysregulation and behavioral analysis of mouse mutants with altered glucocorticoid or mineralocorticoid receptor function. Stress 11 (2008) 321-338
79. Meaney M.J., Aitken D.H., Viau V., Sharma S., and Sarrieau A. Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50 (1989) 597-604
80. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24 (2001) 1161-1192
81. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nat Neurosci 7 (2004) 847-854
82. Weaver I.C., D'Alessio A.C., Brown S.E., Hellstrom I.C., Dymov S., Sharma S., et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 27 (2007) 1756-1768
83. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12 (2009) 342-348
84. McCormick J.A., Lyons V., Jacobson M.D., Noble J., Diorio J., Nyirenda M., et al. 5′-Heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Mol Endocrinol 14 (2000) 506-517
85. Turner J.D., and Muller C.P. Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: identification, and tissue distribution of multiple new human exon 1. J Mol Endocrinol 35 (2005) 283-292
86. Culty M., Thuillier R., Li W., Wang Y., Martinez-Arguelles D.B., Benjamin C.G., et al. In utero exposure to di-(2-ethylhexyl) phthalate exerts both short-term and long-lasting suppressive effects on testosterone production in the rat. Biol Reprod 78 (2008) 1018-1028
87. Davidoff M.S., Middendorff R., Enikolopov G., Riethmacher D., Holstein A.F., and Muller D. Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 167 (2004) 935-944
88. Benton L., Shan L.X., and Hardy M.P. Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 53 (1995) 61-68
89. Koo H.J., and Lee B.M. Toxicokinetic relationship between di(2-ethylhexyl) phthalate (DEHP) and mono(2-ethylhexyl) phthalate in rats. J Toxicol Environ Health A 70 (2007) 383-387
90. Martinez-Arguelles D.B., Culty M., Zirkin B.R., and Papadopoulos V. In utero exposure to di-(2-ethylhexyl) phthalate decreases mineralocorticoid receptor expression in the adult testis. Endocrinology 150 (2009) 5575-5585
91. Stier Jr. C.T., Rocha R., and Chander P.N. Effect of aldosterone and MR blockade on the brain and the kidney. Heart Fail Rev 10 (2005) 53-62
92. Ge R.S., Dong Q., Sottas C.M., Latif S.A., Morris D.J., and Hardy M.P. Stimulation of testosterone production in rat Leydig cells by aldosterone is mineralocorticoid receptor mediated. Mol Cell Endocrinol 243 (2005) 35-42
93. Zennaro M.C., Keightley M.C., Kotelevtsev Y., Conway G.S., Soubrier F., and Fuller P.J. Human mineralocorticoid receptor genomic structure and identification of expressed isoforms. J Biol Chem 270 (1995) 21016-21020
94. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J Neurobiol 36 (1998) 357-378
95. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294 (1990) 76-95
96. Young L.J., Wang Z., Donaldson R., and Rissman E.F. Estrogen receptor alpha is essential for induction of oxytocin receptor by estrogen. Neuroreport 9 (1998) 933-936
97. Kuppers E., Krust A., Chambon P., and Beyer C. Functional alterations of the nigrostriatal dopamine system in estrogen receptor-alpha knockout (ERKO) mice. Psychoneuroendocrinology 33 (2008) 832-838
98. Numan M. Neural basis of maternal behavior in the rat. Psychoneuroendocrinology 13 (1988) 47-62
99. Flanagan-Cato L.M., Calizo L.H., and Daniels D. The synaptic organization of VMH neurons that mediate the effects of estrogen on sexual behavior. Horm Behav 40 (2001) 178-182
100. Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M., and Meaney M.J. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147 (2006) 2909-2915
101. Green S., Kumar V., Krust A., Walter P., and Chambon P. Structural and functional domains of the estrogen receptor. Cold Spring Harb Symp Quant Biol 51 Pt 2 (1986) 751-758
102. Piva R., Gambari R., Zorzato F., Kumar L., and del S.L. Analysis of upstream sequences of the human estrogen receptor gene. Biochem Biophys Res Commun 183 (1992) 996-1002
103. Ottaviano Y.L., Issa J.P., Parl F.F., Smith H.S., Baylin S.B., and Davidson N.E. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54 (1994) 2552-2555
104. Lapidus R.G., Nass S.J., Butash K.A., Parl F.F., Weitzman S.A., Graff J.G., et al. Mapping of ER gene CpG island methylation-specific polymerase chain reaction. Cancer Res 58 (1998) 2515-2519
105. Ferguson A.T., Lapidus R.G., Baylin S.B., and Davidson N.E. Demethylation of the estrogen receptor gene in estrogen receptor-negative breast cancer cells can reactivate estrogen receptor gene expression. Cancer Res 55 (1995) 2279-2283
106. Yang X., Ferguson A.T., Nass S.J., Phillips D.L., Butash K.A., Wang S.M., et al. Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition. Cancer Res 60 (2000) 6890-6894
107. Armenti A.E., Zama A.M., Passantino L., and Uzumcu M. Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats. Toxicol Appl Pharmacol 233 (2008) 286-296
108. Zama A.M., and Uzumcu M. Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes. Endocrinology 150 (2009) 4681-4691
109. Couse J.F., and Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr Rev 20 (1999) 358-417
110. Couse J.F., Yates M.M., Deroo B.J., and Korach K.S. Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146 (2005) 3247-3262
111. Yap O.W., Bhat G., Liu L., and Tollefsbol T.O. Epigenetic modifications of the estrogen receptor beta gene in epithelial ovarian cancer cells. Anticancer Res 29 (2009) 139-144
112. Walton T.J., Li G., Seth R., McArdle S.E., Bishop M.C., and Rees R.C. DNA demethylation and histone deacetylation inhibition co-operate to re-express estrogen receptor beta and induce apoptosis in prostate cancer cell-lines. Prostate 68 (2008) 210-222
113. Jarrard D.F., Kinoshita H., Shi Y., Sandefur C., Hoff D., Meisner L.F., et al. Methylation of the androgen receptor promoter CpG island is associated with loss of androgen receptor expression in prostate cancer cells. Cancer Res 58 (1998) 5310-5314
114. Takahashi S., Inaguma S., Sakakibara M., Cho Y.M., Suzuki S., Ikeda Y., et al. DNA methylation in the androgen receptor gene promoter region in rat prostate cancers. Prostate 52 (2002) 82-88
115. Nakayama T., Watanabe M., Suzuki H., Toyota M., Sekita N., Hirokawa Y., et al. Epigenetic regulation of androgen receptor gene expression in human prostate cancers. Lab Invest 80 (2000) 1789-1796
116. Schulz W.A., and Hoffmann M.J. Epigenetic mechanisms in the biology of prostate cancer. Semin Cancer Biol 19 (2009) 172-180
117. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437 (2005) 436-439
118. Nelson W.G. Prostate cancer prevention. Curr Opin Urol 17 (2007) 157-167
119. Hmadcha A., Bedoya F.J., Sobrino F., and Pintado E. Methylation-dependent gene silencing induced by interleukin 1beta via nitric oxide production. J Exp Med 190 (1999) 1595-1604
120. Bastian P.J., Yegnasubramanian S., Palapattu G.S., Rogers C.G., Lin X., De Marzo A.M., et al. Molecular biomarker in prostate cancer: the role of CpG island hypermethylation. Eur Urol 46 (2004) 698-708
121. Martin D.I., Cropley J.E., and Suter C.M. Environmental influence on epigenetic inheritance at the Avy allele. Nutr Rev 66 Suppl 1 (2008) S12-S14
122. Liu L., Li Y., and Tollefsbol T.O. Gene-environment interactions and epigenetic basis of human diseases. Curr Issues Mol Biol 10 (2008) 25-36
123. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117 (2002) 15-23
124. Warnecke P.M., Stirzaker C., Song J., Grunau C., Melki J.R., and Clark S.J. Identification and resolution of artifacts in bisulfite sequencing. Methods 27 (2002) 101-107
125. Ho S.M., and Tang W.Y. Techniques used in studies of epigenome dysregulation due to aberrant DNA methylation: an emphasis on fetal-based adult diseases. Reprod Toxicol 23 (2007) 267-282
126. Beck S., and Rakyan V.K. The methylome: approaches for global DNA methylation profiling. Trends Genet 24 (2008) 231-237
127. Brena R.M., Huang T.H., and Plass C. Quantitative assessment of DNA methylation: potential applications for disease diagnosis, classification, and prognosis in clinical settings. J Mol Med 84 (2006) 365-377
128. Taylor K.H., Kramer R.S., Davis J.W., Guo J., Duff D.J., Xu D., et al. Ultradeep bisulfite sequencing analysis of DNA methylation patterns in multiple gene promoters by 454 sequencing. Cancer Res 67 (2007) 8511-8518
129. Gitan R.S., Shi H., Chen C.M., Yan P.S., and Huang T.H. Methylation-specific oligonucleotide microarray: a new potential for high-throughput methylation analysis. Genome Res 12 (2002) 158-164
130. Graf S., Nielsen F.G., Kurtz S., Huynen M.A., Birney E., Stunnenberg H., et al. Optimized design and assessment of whole genome tiling arrays. Bioinformatics 23 (2007) i195-i204
131. Hatada I., Hayashizaki Y., Hirotsune S., Komatsubara H., and Mukai T. A genomic scanning method for higher organisms using restriction sites as landmarks. Proc Natl Acad Sci USA 88 (1991) 9523-9527
132. Huang T.H., Laux D.E., Hamlin B.C., Tran P., Tran H., and Lubahn D.B. Identification of DNA methylation markers for human breast carcinomas using the methylation-sensitive restriction fingerprinting technique. Cancer Res 57 (1997) 1030-1034
133. Wu M., and Ho S.M. PMP24, a gene identified by MSRF, undergoes DNA hypermethylation-associated gene silencing during cancer progression in an LNCaP model. Oncogene 23 (2004) 250-259
134. Oakes C.C., La S.S., Smiraglia D.J., Robaire B., and Trasler J.M. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 307 (2007) 368-379
135. Rouillard J.M., Erson A.E., Kuick R., Asakawa J., Wimmer K., Muleris M., et al. Virtual genome scan: a tool for restriction landmark-based scanning of the human genome. Genome Res 11 (2001) 1453-1459
136. Smiraglia D.J., Kazhiyur-Mannar R., Oakes C.C., Wu Y.Z., Liang P., Ansari T., et al. Restriction landmark genomic scanning (RLGS) spot identification by second generation virtual RLGS in multiple genomes with multiple enzyme combinations. BMC Genomics 8 (2007) 446
137. Costello J.F., Hong C., Plass C., and Smiraglia D.J. Restriction landmark genomic scanning: analysis of CpG islands in genomes by 2D gel electrophoresis. Methods Mol Biol 507 (2009) 131-148