Mapping ERβ Genomic Binding Sites Reveals Unique Genomic Features and Identifies EBF1 as an ERβ Interactor

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Le, Thien P ^a   Sun, Miao ^b   Luo, Xin ^b   Kraus, W Lee ^b   Greene, Geoffrey L ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; EARLY B CELL FACTOR 1; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GFI PROTEIN; REST PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; BINDING SITE; CDKN1A GENE; CELL PROLIFERATION; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE MAPPING; GENE TARGETING; GENETIC ASSOCIATION; KLF10 GENE; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA ANALYSIS; SEQUENCE ANALYSIS; UPREGULATION;

BINDING SITES; CELL LINE; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GENE DELETION; GENE EXPRESSION; GENE ONTOLOGY; GENOME, HUMAN; HUMANS; TRANS-ACTIVATORS;

EID: 84881361229     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071355     Document Type: Article

References (59)

1. Hall JM, Couse JF, Korach KS (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem. 276(40): p.36869-72.
2. Heldring N, Pike A, Andersson S, Matthews J, Cheng G,et al. (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 87(3): p.905-31.
3. Murphy LC, Leygue E (2012) The Role of Estrogen Receptor-beta in Breast Cancer. Semin Reprod Med. 30(01): p.8.
4. Deroo BJ, Buensuceso AV (2010) Minireview: Estrogen receptor-beta: mechanistic insights from recent studies. Mol Endocrinol. 24(9): p.1703-14.
5. Weihua Z, Makela S, Andersson LC, Salmi S, Saji S,et al. (2001) A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA. 98(11): p.6330-5.
6. Deroo BJ, Korach KS (2006) Estrogen receptors and human disease. J Clin Invest. 116(3): p.561-70.
7. Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocrine Reviews. 20(3): p.358-417.
8. Krezel W, Dupont S, Krust A, Chambon P, Chapman PF (2001) Increased anxiety and synaptic plasticity in estrogen receptor beta-deficient mice. Proc Natl Acad Sci USA. 98(21): p.12278-82.
9. Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson JA,et al. (2000) Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO). Proc Natl Acad Sci USA. 97(26): p.14737-41.
10. Hall JM, McDonnell DP (1999) The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology. 140(12): p.5566-78.
11. McInerney EM, Weis KE, Sun J, Mosselman S, Katzenellenbogen BS (1998) Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology. 139(11): p.4513-22.
12. Tremblay GB, Tremblay A, Copeland NG, Gilbert DJ, Jenkins NA,et al. (1997) Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Molecular endocrinology (Baltimore, Md). 11(3): p.353-65.
13. Picard N, Charbonneau C, Sanchez M, Licznar A, Busson M,et al. (2008) Phosphorylation of activation function-1 regulates proteasome-dependent nuclear mobility and E6-associated protein ubiquitin ligase recruitment to the estrogen receptor beta. Molecular Endocrinology. 22(2): p.317-30.
14. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR,et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet. 38(11): p.1289-97.
15. Welboren W-J, van Driel MA, Janssen-Megens EM, van Heeringen SJ, Sweep FC,et al. (2009) ChIP-Seq of ERalpha and RNA polymerase II defines genes differentially responding to ligands. EMBO J. 28(10): p.1418-28.
16. Charn TH, Liu ET-B, Chang EC, Lee YK, Katzenellenbogen JA,et al. (2010) Genome-wide dynamics of chromatin binding of estrogen receptors alpha and beta: mutual restriction and competitive site selection. Molecular endocrinology (Baltimore, Md). 24(1): p.47-59.
17. Harris HA (2007) Estrogen receptor-beta: recent lessons from in vivo studies. Molecular Endocrinology. 21(1): p.1-13.
18. Bianco NR, Perry G, Smith MA, Templeton DJ, Montano MM (2003) Functional implications of antiestrogen induction of quinone reductase: inhibition of estrogen-induced deoxyribonucleic acid damage. Molecular endocrinology (Baltimore, Md). 17(7): p.1344-55.
19. Chang EC, Frasor J, Komm B, Katzenellenbogen BS (2006) Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology. 147(10): p.4831-42.
20. Chen M, Ni J, Chang H-C, Lin C-Y, Muyan M,et al. (2009) CCDC62/ERAP75 functions as a coactivator to enhance estrogen receptor beta-mediated transactivation and target gene expression in prostate cancer cells. Carcinogenesis. 30(5): p.841-50.
21. Hurtado A, Pinós T, Barbosa-Desongles A, López-Avilés S, Barquinero J,et al. (2008) Estrogen receptor beta displays cell cycle-dependent expression and regulates the G1 phase through a non-genomic mechanism in prostate carcinoma cells. Cellular oncology: the official journal of the International Society for Cellular Oncology. 30(4): p.349-65.
22. Pravettoni A, Mornati O, Martini PGV, Marino M, Colciago A,et al. (2007) Estrogen receptor beta (ERbeta) and inhibition of prostate cancer cell proliferation: studies on the possible mechanism of action in DU145 cells. Molecular and cellular endocrinology. 263(1-2): p.46-54.
23. Snyder MA, Smejkalova T, Forlano PM, Woolley CS (2010) Multiple ERI^2 antisera label in ERI^2 knockout and null mouse tissues. Journal of neuroscience methods. 188(2): p.226-234.
24. Liu Y, Gao H, Marstrand TT, Ström A, Valen E,et al. (2008) The genome landscape of ERalpha- and ERbeta-binding DNA regions. Proc Natl Acad Sci USA. 105(7): p.2604-9.
25. Vivar OI, Zhao X, Saunier EF, Griffin C, Mayba OS,et al. (2010) Estrogen receptor beta binds to and regulates three distinct classes of target genes. Journal of Biological Chemistry. 285(29): p.22059-66.
26. Tee MK, Rogatsky I, Tzagarakis-Foster C, Cvoro A, An J,et al. (2004) Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors alpha and beta. Mol Biol Cell. 15(3): p.1262-72.
27. Matthews J, Wihlén B, Tujague M, Wan J, Ström A,et al. (2006) Estrogen receptor (ER) beta modulates ERalpha-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Molecular endocrinology (Baltimore, Md). 20(3): p.534-43.
28. Monroe DG, Getz BJ, Johnsen SA, Riggs BL, Khosla S,et al. (2003) Estrogen receptor isoform-specific regulation of endogenous gene expression in human osteoblastic cell lines expressing either ERalpha or ERbeta. J. Cell. Biochem. 90(2): p.315-26.
29. Monroe DG, Secreto FJ, Subramaniam M, Getz BJ, Khosla S,et al. (2005) Estrogen receptor alpha and beta heterodimers exert unique effects on estrogen- and tamoxifen-dependent gene expression in human U2OS osteosarcoma cells. Molecular endocrinology (Baltimore, Md). 19(6): p.1555-68.
30. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR,et al. (2004) Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER) alpha or ERbeta in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology. 145(7): p.3473-86.
31. Walker MP, Zhang M, Le TP, Wu P, Lainé M,et al. (2011) RAC3 is a pro-migratory co-activator of ERα. Oncogene. p.1-11.
32. Hah N, Danko CG, Core L, Waterfall JJ, Siepel A,et al. (2011) A Rapid, Extensive, and Transient Transcriptional Response to Estrogen Signaling in Breast Cancer Cells. Cell. 145(4): p.622-634.
33. Oesterreich S, Zhang P, Guler RL, Sun X, Curran EM,et al. (2001) Re-expression of estrogen receptor alpha in estrogen receptor alpha-negative MCF-7 cells restores both estrogen and insulin-like growth factor-mediated signaling and growth. Cancer Res. 61(15): p.5771-7.
34. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E,et al. (2008) Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat Methods. 5(9): p.829-34.
35. Ji X, Li W, Song J, Wei L, Liu XS (2006) CEAS: cis-regulatory element annotation system. Nucleic Acids Res. 34(Web Server issue): p. W551-4.
36. Frith MC, Fu Y, Yu L, Chen J-F, Hansen U,et al. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res. 32(4): p.1372-81.
37. Core LJ, Waterfall JJ, Lis JT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science. 322(5909): p.1845-8.
38. Liao D (2009) Emerging roles of the EBF family of transcription factors in tumor suppression. Molecular Cancer Research. 7(12): p.1893-901.
39. Cheung E, Kraus WL (2010) Genomic analyses of hormone signaling and gene regulation. Annu Rev Physiol. 72: p.191-218.
40. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR,et al. (2012) Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 481(7381): p.389-93.
41. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA. 93(12): p.5925-30.
42. Zhao LY, Niu Y, Santiago A, Liu J, Albert SH,et al. (2006) An EBF3-mediated transcriptional program that induces cell cycle arrest and apoptosis. Cancer Res. 66(19): p.9445-52.
43. Frisch RE (1987) Body fat, menarche, fitness and fertility. Hum Reprod. 2(6): p.521-33.
44. Masood S (1992) Estrogen and progesterone receptors in cytology: a comprehensive review. Diagn Cytopathol. 8(5): p.475-91.
45. Gimble JM, Robinson CE, Clarke SL, Hill MR (1998) Nuclear hormone receptors and adipogenesis. Crit Rev Eukaryot Gene Expr. 8(2): p.141-68.
46. Liberg D, Sigvardsson M, Akerblad P (2002) The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers. Molecular and Cellular Biology. 22(24): p.8389-97.
47. Heim M, Frank O, Kampmann G, Sochocky N, Pennimpede T,et al. (2004) The phytoestrogen genistein enhances osteogenesis and represses adipogenic differentiation of human primary bone marrow stromal cells. Endocrinology. 145(2): p.848-59.
48. Okazaki R, Inoue D, Shibata M, Saika M, Kido S,et al. (2002) Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology. 143(6): p.2349-56.
49. Dang ZC, van Bezooijen RL, Karperien M, Papapoulos SE, Löwik CWGM (2002) Exposure of KS483 cells to estrogen enhances osteogenesis and inhibits adipogenesis. J Bone Miner Res. 17(3): p.394-405.
50. Zhang M, Ikeda K, Xu J-W, Yamori Y, Gao X-M,et al. (2009) Genistein suppresses adipogenesis of 3T3-L1 cells via multiple signal pathways. Phytother Res. 23(5): p.713-8.
51. Jeong S, Yoon M (2011) 17β-Estradiol inhibition of PPARγ-induced adipogenesis and adipocyte-specific gene expression. Acta Pharmacol Sin. 32(2): p.230-8.
52. Akerblad P, Lind U, Liberg D, Bamberg K, Sigvardsson M (2002) Early B-cell factor (O/E-1) is a promoter of adipogenesis and involved in control of genes important for terminal adipocyte differentiation. Mol Cell Biol. 22(22): p.8015-25.
53. Akerblad P, Mansson R, Lagergren A, Westerlund S, Basta B,et al. (2005) Gene expression analysis suggests that EBF-1 and PPARgamma2 induce adipogenesis of NIH-3T3 cells with similar efficiency and kinetics. Physiological Genomics. 23(2): p.206-16.
54. Medina KL, Strasser A, Kincade PW (2000) Estrogen influences the differentiation, proliferation, and survival of early B-lineage precursors. Blood. 95(6): p.2059-67.
55. Medina KL, Garrett KP, Thompson LF, Rossi MI, Payne KJ,et al. (2001) Identification of very early lymphoid precursors in bone marrow and their regulation by estrogen. Nat Immunol. 2(8): p.718-24.
56. Medina KL, Kincade PW (1994) Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA. 91(12): p.5382-6.
57. Hill L, Jeganathan V, Chinnasamy P, Grimaldi C, Diamond B (2011) Differential roles of estrogen receptors α and β in control of B-cell maturation and selection. Molecular medicine (Cambridge, Mass). 17(3-4): p.211-20.
58. Smithson G, Beamer WG, Shultz KL, Christianson SW, Shultz LD,et al. (1994) Increased B lymphopoiesis in genetically sex steroid-deficient hypogonadal (hpg) mice. J Exp Med. 180(2): p.717-20.
59. Islander U, Erlandsson MC, Hasséus B, Jonsson CA, Ohlsson C,et al. (2003) Influence of oestrogen receptor alpha and beta on the immune system in aged female mice. Immunology. 110(1): p.149-57.