Oestrogen receptor β regulates epigenetic patterns at specific genomic loci through interaction with thymine DNA glycosylase

Epigenetics and Chromatin

Volumn 9, Issue 1, 2016, Pages

  Liu, Yun ^a   Duong, William ^b,f   Krawczyk, Claudia ^b   Bretschneider, Nancy ^c   Borbély, Gábor ^d   Varshney, Mukesh ^e   Zinser, Christian ^d   Schär, Primo ^b   Rüegg, Joëlle ^b,d,e  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF BASEL   (Switzerland)

^c Genomatix GmbH   (Germany)

^d Swedish Toxicology Sciences Research Center (Swetox)   (Sweden)

^e KAROLINSKA INSTITUTE   (Sweden)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

DNA methylation; Mouse embryonic fibroblasts; Mouse embryonic stem cells; Oestrogen receptor ; Reduced representation bisulfite sequencing; Thymine DNA glycosylase

Indexed keywords

BISULFITE; DNA; ESTROGEN RECEPTOR BETA; THYMINE DNA GLYCOSYLASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EPIGENETICS; FIBROBLAST; GENE EXPRESSION; GENE LOCUS; GENE ONTOLOGY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

EID: 84958244058     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-016-0055-7     Document Type: Article

References (64)

1. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6-21.
2. Chen T, Dent SY. Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat Rev Genet. 2014;15(2):93-106. doi: 10.1038/nrg3607.
3. Chen M, Zhang L. Epigenetic mechanisms in developmental programming of adult disease. Drug Discovery Today. 2011;16(23-24):1007-18. doi: 10.1016/j.drudis.2011.09.008.
4. Patra SK, Patra A, Rizzi F, Ghosh TC, Bettuzzi S. Demethylation of (Cytosine-5-C-methyl) DNA and regulation of transcription in the epigenetic pathways of cancer development. Cancer Metastasis Rev. 2008;27(2):315-34.
5. Saitou M, Kagiwada S, Kurimoto K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development. 2012;139(1):15-31. doi: 10.1242/dev.050849.
6. Coskun V, Tsoa R, Sun YE. Epigenetic regulation of stem cells differentiating along the neural lineage. Curr Opin Neurobiol. 2012;22(5):762-7. doi: 10.1016/j.conb.2012.07.001.
7. Guo JU, Su Y, Zhong C, Ming GL, Song H. Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle. 2011;10(16):2662-8.
8. Shen L, Zhang Y. 5-Hydroxymethylcytosine: generation, fate, and genomic distribution. Curr Opin Cell Biol. 2013;25(3):289-96. doi: 10.1016/j.ceb.2013.02.017.
9. Gao F, Xia Y, Wang J, Luo H, Gao Z, Han X, et al. Integrated detection of both 5-mC and 5-hmC by high-throughput tag sequencing technology highlights methylation reprogramming of bivalent genes during cellular differentiation. Epigenetics Off J DNA Methylation Soc. 2013;8(4):421-30.
10. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell. 2007;128(4):669-81. doi: 10.1016/j.cell.2007.01.033.
11. Maiti A, Drohat AC. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem. 2011;286(41):35334-8. doi: 10.1074/jbc.C111.284620.
12. Jacobs AL, Schar P. DNA glycosylases: in DNA repair and beyond. Chromosoma. 2012;121(1):1-20. doi: 10.1007/s00412-011-0347-4.
13. Cortazar D, Kunz C, Selfridge J, Lettieri T, Saito Y, MacDougall E, et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature. 2011;470(7334):419-23. doi: 10.1038/nature09672.
14. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, Cigliano A, et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell. 2011;146(1):67-79. doi: 10.1016/j.cell.2011.06.020.
15. Shen L, Wu H, Diep D, Yamaguchi S, D'Alessio AC, Fung HL, et al. Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell. 2013;153(3):692-706. doi: 10.1016/j.cell.2013.04.002.
16. Song CX, Szulwach KE, Dai Q, Fu Y, Mao SQ, Lin L, et al. Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell. 2013;153(3):678-91. doi: 10.1016/j.cell.2013.04.001.
17. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schubeler D. Identification of genetic elements that autonomously determine DNA methylation states. Nat Genet. 2011;43(11):1091-7. doi: 10.1038/ng.946.
18. Feldmann A, Ivanek R, Murr R, Gaidatzis D, Burger L, Schubeler D. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet. 2013;9(12):e1003994. doi: 10.1371/journal.pgen.1003994.
19. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature. 2011;480(7378):490-5. doi: 10.1038/nature10716.
20. Schmitz KM, Mayer C, Postepska A, Grummt I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 2010;24(20):2264-9. doi: 10.1101/gad.590910.
21. Zhang Z, Tang H, Wang Z, Zhang B, Liu W, Lu H, et al. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol Cancer. 2011;10:124. doi: 10.1186/1476-4598-10-124.
22. Guseva N, Mondal T, Kanduri C. Antisense noncoding RNA promoter regulates the timing of de novo methylation of an imprinting control region. Dev Biol. 2012;361(2):403-11. doi: 10.1016/j.ydbio.2011.11.005.
23. Arab K, Park YJ, Lindroth AM, Schafer A, Oakes C, Weichenhan D, et al. Long noncoding RNA TARID directs demethylation and activation of the tumor suppressor TCF21 via GADD45A. Mol Cell. 2014;55(4):604-14. doi: 10.1016/j.molcel.2014.06.031.
24. Martens JH, Rao NA, Stunnenberg HG. Genome-wide interplay of nuclear receptors with the epigenome. Biochim Biophys Acta. 2011;1812(8):818-23. doi: 10.1016/j.bbadis.2010.10.005.
25. Ruegg J, Cai W, Karimi M, Kiss NB, Swedenborg E, Larsson C, et al. Epigenetic regulation of glucose transporter 4 by estrogen receptor beta. Mol Endocrinol. 2011;25(12):2017-28. doi: 10.1210/me.2011-1054.
26. Thomassin H, Flavin M, Espinas ML, Grange T. Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO J. 2001;20(8):1974-83.
27. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature. 2008;452(7183):45-50.
28. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, et al. Transient cyclical methylation of promoter DNA. Nature. 2008;452(7183):112-5. doi: 10.1038/nature06640.
29. Kim MS, Kondo T, Takada I, Youn MY, Yamamoto Y, Takahashi S, et al. DNA demethylation in hormone-induced transcriptional derepression. Nature. 2009;461(7266):1007-12. doi: 10.1038/nature08456.
30. Marques M, Laflamme L, Gaudreau L. Estrogen receptor alpha can selectively repress dioxin receptor-mediated gene expression by targeting DNA methylation. Nucleic Acids Res. 2013;. doi: 10.1093/nar/gkt595.
31. Zhao C, Dahlman-Wright K, Gustafsson JA. Estrogen receptor beta: an overview and update. Nucl Recept Signal. 2008;6:e003. doi: 10.1621/nrs.06003.
32. Barros RP, Gustafsson JA. Estrogen receptors and the metabolic network. Cell Metab. 2011;14(3):289-99. doi: 10.1016/j.cmet.2011.08.005.
33. Metivier R, Penot G, Hubner MR, Reid G, Brand H, Kos M, et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell. 2003;115(6):751-63.
34. Ho SM, Johnson A, Tarapore P, Janakiram V, Zhang X, Leung YK. Environmental epigenetics and its implication on disease risk and health outcomes. ILAR J. 2012;53(3-4):289-305. doi: 10.1093/ilar.53.3-4.289.
35. Bernal AJ, Jirtle RL. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res A Clin Mol Teratol. 2010;88(10):938-44. doi: 10.1002/bdra.20685.
36. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature. 2008;454(7205):766-70. doi: 10.1038/nature07107.
37. Grober OM, Mutarelli M, Giurato G, Ravo M, Cicatiello L, De Filippo MR, et al. Global analysis of estrogen receptor beta binding to breast cancer cell genome reveals an extensive interplay with estrogen receptor alpha for target gene regulation. BMC Genom. 2011;12:36. doi: 10.1186/1471-2164-12-36.
38. Sengupta PK, Fargo J, Smith BD. The RFX family interacts at the collagen (COL1A2) start site and represses transcription. J Biol Chem. 2002;277(28):24926-37. doi: 10.1074/jbc.M111712200.
39. Zhao M, Sun Y, Gao F, Wu X, Tang J, Yin H, et al. Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4 + T cells. J Autoimmun. 2010;35(1):58-69. doi: 10.1016/j.jaut.2010.02.002.
40. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, Bauer C, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell. 2013;152(5):1146-59. doi: 10.1016/j.cell.2013.02.004.
41. Faulds MH, Pettersson K, Gustafsson JA, Haldosen LA. Cross-talk between ERs and signal transducer and activator of transcription 5 is E2 dependent and involves two functionally separate mechanisms. Mol Endocrinol. 2001;15(11):1929-40. doi: 10.1210/mend.15.11.0726.
42. Lee SK, Choi HS, Song MR, Lee MO, Lee JW. Estrogen receptor, a common interaction partner for a subset of nuclear receptors. Mol Endocrinol. 1998;12(8):1184-92. doi: 10.1210/mend.12.8.0146.
43. Ruegg J, Swedenborg E, Wahlstrom D, Escande A, Balaguer P, Pettersson K, et al. The transcription factor aryl hydrocarbon receptor nuclear translocator functions as an estrogen receptor beta-selective coactivator, and its recruitment to alternative pathways mediates antiestrogenic effects of dioxin. Mol Endocrinol. 2008;22(2):304-16.
44. Chen D, Lucey MJ, Phoenix F, Lopez-Garcia J, Hart SM, Losson R, et al. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor alpha. J Biol Chem. 2003;278(40):38586-92.
45. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011;333(6047):1303-7. doi: 10.1126/science.1210944.
46. Hardeland U, Steinacher R, Jiricny J, Schar P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 2002;21(6):1456-64. doi: 10.1093/emboj/21.6.1456.
47. Legler J, van den Brink CE, Brouwer A, Murk AJ, van der Saag PT, Vethaak AD, et al. Development of a stably transfected estrogen receptor-mediated luciferase reporter gene assay in the human T47D breast cancer cell line. Toxicol Sci Off J Soc Toxicol. 1999;48(1):55-66.
48. Thillainadesan G, Chitilian JM, Isovic M, Ablack JN, Mymryk JS, Tini M, et al. TGF-beta-dependent active demethylation and expression of the p15ink4b tumor suppressor are impaired by the ZNF217/CoREST complex. Mol Cell. 2012;46(5):636-49. doi: 10.1016/j.molcel.2012.03.027.
49. Leger H, Smet-Nocca C, Attmane-Elakeb A, Morley-Fletcher S, Benecke AG, Eilebrecht S. A TDG/CBP/RARalpha ternary complex mediates the retinoic acid-dependent expression of DNA methylation-sensitive genes. Genomics Proteomics Bioinformatics. 2014;12(1):8-18. doi: 10.1016/j.gpb.2013.11.001.
50. Ruegg J, Cai W, Karimi M, Kiss NB, Swedenborg E, Larsson C, et al. Epigenetic regulation of glucose transporter 4 by estrogen receptor beta. Mol Endocrinol. 2011;25(12):2017-28. doi: 10.1210/me.2011-1054.
51. Lucey MJ, Chen D, Lopez-Garcia J, Hart SM, Phoenix F, Al-Jehani R, et al. T:G mismatch-specific thymine-DNA glycosylase (TDG) as a coregulator of transcription interacts with SRC1 family members through a novel tyrosine repeat motif. Nucleic Acids Res. 2005;33(19):6393-404. doi: 10.1093/nar/gki940.
52. Chang EC, Frasor J, Komm B, Katzenellenbogen BS. Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology. 2006;147(10):4831-42. doi: 10.1210/en.2006-0563.
53. Liu Z, Merkurjev D, Yang F, Li W, Oh S, Friedman MJ, et al. Enhancer activation requires trans-recruitment of a mega transcription factor complex. Cell. 2014;159(2):358-73. doi: 10.1016/j.cell.2014.08.027.
54. Franco MM, Prickett AR, Oakey RJ. The role of CCCTC-binding factor (CTCF) in genomic imprinting, development, and reproduction. Biol Reprod. 2014;91(5):125. doi: 10.1095/biolreprod.114.122945.
55. Ginno PA, Lott PL, Christensen HC, Korf I, Chedin F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell. 2012;45(6):814-25. doi: 10.1016/j.molcel.2012.01.017.
56. Kunz C, Focke F, Saito Y, Schuermann D, Lettieri T, Selfridge J, et al. Base excision by thymine DNA glycosylase mediates DNA-directed cytotoxicity of 5-fluorouracil. PLoS Biol. 2009;7(4):e91. doi: 10.1371/journal.pbio.1000091.
57. Delaunay F, Pettersson K, Tujague M, Gustafsson JA. Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol Pharmacol. 2000;58(3):584-90.
58. Cortazar D, Kunz C, Selfridge J, Lettieri T, Saito Y, Macdougall E et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature. doi: 10.1038/nature09672.
59. Ying QL, Smith AG. Defined conditions for neural commitment and differentiation. Methods Enzymol. 2003;365:327-41.
60. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, et al. The ground state of embryonic stem cell self-renewal. Nature. 2008;453(7194):519-23. doi: 10.1038/nature06968.
61. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat Protoc. 2011;6(4):468-81. doi: 10.1038/nprot.2010.190.
62. Team RC. R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2014.
63. Steinacher R, Schar P. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr Biol. 2005;15(7):616-23. doi: 10.1016/j.cub.2005.02.054
64. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207-10