Genome-wide dynamics of chromatin binding of estrogen receptors α and β: Mutual restriction and competitive site selection

Molecular Endocrinology

Volumn 24, Issue 1, 2010, Pages 47-59

  Charn, Tze Howe ^a   Liu, Edison Tak Bun ^d   Chang, Edmund C ^b   Lee, Yew Kok ^d   Katzenellenbogen, John A ^a,c   Katzenellenbogen, Benita S ^b  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HORMONE; LIGAND; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CELL STRAIN MCF 7; CELL TYPE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COMPETITION; ESTROGEN RESPONSIVE ELEMENT; GENE CONTROL; GENE EXPRESSION; GENOME; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR BINDING; SEQUENCE ANALYSIS;

BINDING, COMPETITIVE; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; LIGANDS; OXAZOLES; PYRAZOLES; RESPONSE ELEMENTS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 73549104043     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2009-0252     Document Type: Article

References (52)

1. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ 2006 Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126:789-799
2. Deroo BJ, Korach KS 2006 Estrogen receptors and human disease. J Clin Invest 116:561-570
3. Nilsson S, MäkeläS, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA 2001 Mechanisms of estrogen action. Physiol Rev 81:1535-1565
4. Chang EC, Frasor J, Komm B, Katzenellenbogen BS 2006 Impact of estrogen receptor β on gene networks regulated by estrogen receptor α in breast cancer cells. Endocrinology 147:4831-4842
5. Chang EC, Charn TH, Park SH, Helferich WG, Komm B, Katzenellenbogen JA, Katzenellenbogen BS 2008 Estrogen receptors α and β as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol Endocrinol 22:1032-1043
6. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS 2003 Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 144:4562-4574
7. Paruthiyil S, Parmar H, Kerekatte V, Cunha GR, Firestone GL, Leitman DC 2004 Estrogen receptor β inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res 64:423-428
8. Ström A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA 2004 Estrogen receptor β inhibits 17β-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci USA 101:1566-1571
9. Williams C, Edvardsson K, Lewandowski SA, Ström A, Gustafsson JA 2008 A genome-wide study of the repressive effects of estrogen receptor β on estrogen receptor α signaling in breast cancer cells. Oncogene 27:1019-1032
10. Frasor J, Chang EC, Komm B, Lin CY, Vega VB, Liu ET, Miller LD, Smeds J, Bergh J, Katzenellenbogen BS 2006 Gene expression preferentially regulated by tamoxifen in breast cancer cells and correlations with clinical outcome. Cancer Res 66:7334-7340
11. Kraichely DM, Sun J, Katzenellenbogen JA, Katzenellenbogen BS 2000 Conformational changes and coactivator recruitment by novel ligands for estrogen receptor-α and estrogen receptor-β: correlations with biological character and distinct differences among SRC coactivator family members. Endocrinology 141: 3534-3545
12. Malamas MS, Manas ES, McDevitt RE, Gunawan I, Xu ZB, Collini MD, Miller CP, Dinh T, Henderson RA, Keith Jr JC, Harris HA 2004 Design and synthesis of aryl diphenolic azoles as potent and selective estrogen receptor-β ligands. J Med Chem 47:5021-5040
13. Meyers MJ, Sun J, Carlson KE, Katzenellenbogen BS, Katzenellenbogen JA 1999 Estrogen receptor subtype-selective ligands: asymmetric synthesis and biological evaluation of cis- and trans-5,11-dialkyl-5,6,11, 12-tetrahydrochrysenes. J Med Chem 42:2456-2468
14. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA 2000 Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-α- selective agonists. J Med Chem 43:4934-4947
15. Katzenellenbogen BS, Frasor J 2004 Therapeutic targeting in the estrogen receptor hormonal pathway. Semin Oncol 31:28-38
16. Kurebayashi J, Otsuki T, Kunisue H, Tanaka K, Yamamoto S, Sonoo H 2000 Expression levels of estrogen receptor-α, estrogen receptor-β, coactivators, and corepressors in breast cancer. Clin Cancer Res 6:512-518
17. Saji S, Hirose M, Toi M 2005 Clinical significance of estrogen receptor beta in breast cancer. Cancer Chemother Pharmacol 56(Suppl 1):21-26
18. Shaaban AM, O'Neill PA, Davies MP, Sibson R, West CR, Smith PH, Foster CS 2003 Declining estrogen receptor-β expression defines malignant progression of human breast neoplasia. Am J Surg Pathol 27:1502-1512
19. Speirs V, Carder PJ, Lane S, Dodwell D, Lansdown MR, Hanby AM 2004 Oestrogen receptor β: what it means for patients with breast cancer. Lancet Oncol 5:174-181
20. Palmieri C, Cheng GJ, Saji S, Zelada-Hedman M, Wärri A, Weihua Z, Van Noorden S, Wahlstrom T, Coombes RC, Warner M, Gustafsson JA 2002 Estrogen receptor β in breast cancer. Endocr Relat Cancer 9:1-13
21. Roger P, Sahla ME, MäkeläS, Gustafsson JA, Baldet P, Rochefort H 2001 Decreased expression of estrogen receptor β protein in proliferative preinvasive mammary tumors. Cancer Res 61:2537-2541
22. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR, Katzenellenbogen BS 2004 Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res 64:1522-1533
23. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR, Katzenellenbogen BS 2004 Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER)α or ERβ in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology 145:3473-3486
24. Lin CY, Vega VB, Thomsen JS, Zhang T, Kong SL, Xie M, Chiu KP, Lipovich L, Barnett DH, Stossi F, Yeo A, George J, Kuznetsov VA, Lee YK, Charn TH, Palanisamy N, Miller LD, Cheung E, Katzenellenbogen BS, Ruan Y, Bourque G, Wei CL, Liu ET 2007 Whole-genome cartography of estrogen receptor α binding sites. PLoS Genet 3:e87
25. Kian Tee M, Rogatsky I, Tzagarakis-Foster C, Cvoro A, An J, Christy RJ, Yamamoto KR, Leitman DC 2004 Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors α and β. Mol Biol Cell 15:1262-1272
26. Lindberg MK, Movérare S, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA, Ohlsson C 2003 Estrogen receptor (ER)-β reduces ERα-regulated gene transcription, supporting a "ying yang" relationship between ERα and ERβ in mice. Mol Endocrinol 17:203-208
27. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M 2006 Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38:1289-1297
28. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M 2005 Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33-43
29. Vega VB, Lin CY, Lai KS, Kong SL, Xie M, Su X, Teh HF, Thomsen JS, Yeo AL, Sung WK, Bourque G, Liu ET 2006 Multiplatform genome-wide identification and modeling of functional human estrogen receptor binding sites. Genome Biol 7:R82
30. Li X, Huang J, Yi P, Bambara RA, Hilf R, Muyan M 2004 Single-chain estrogen receptors (ERs) reveal that the ERα/β heterodimer emulates functions of the ERα dimer in genomic estrogen signaling pathways. Mol Cell Biol 24:7681-7694
31. Cowley SM, Hoare S, Mosselman S, Parker MG 1997 Estrogen receptors α and β form heterodimers on DNA. J Biol Chem 272:19858-19862
32. Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S 1997 Human estrogen receptor β binds DNA in a manner similar to and dimerizes with estrogen receptor α. J Biol Chem 272:25832-25838
33. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA 1997 Mouse estrogen receptor beta forms estrogen response element-binding heterodimers with estrogen receptor α. Mol Endocrinol 11:1486-1496
34. Schultz JR, Loven MA, Melvin VM, Edwards DP, Nardulli AM 2002 Differential modulation of DNA conformation by estrogen receptors α and β. J Biol Chem 277:8702-8707
35. Jisa E, Jungbauer A 2003 Kinetic analysis of estrogen receptor homo-and heterodimerization in vitro. J Steroid Biochem Mol Biol 84:141-148
36. Paulmurugan R, Tamrazi A, Katzenellenbogen JA, Katzenellenbogen BS, Gambhir SS 2008 A human estrogen receptor (ER)α mutation with differential responsiveness to nonsteroidal ligands: novel approaches for studying mechanism of ER action. Mol Endocrinol 22:1552-1564
37. Powell E, Xu W 2008 Intermolecular interactions identify ligand-selective activity of estrogen receptor α/β dimers. Proc Natl Acad Sci USA 105:19012-19017
38. Kininis M, Chen BS, Diehl AG, Isaacs GD, Zhang T, Siepel AC, Clark AG, Kraus WL 2007 Genomic analyses of transcription factor binding, histone acetylation, and gene expression reveal mechanistically distinct classes of estrogen-regulated promoters. Mol Cell Biol 27:5090-5104
39. Liu Y, Gao H, Marstrand TT, Ström A, Valen E, Sandelin A, Gustafsson JA, Dahlman-Wright K 2008 The genome landscape of ERα- and ERβ-binding DNA regions. Proc Natl Acad Sci USA 105:2604-2609
40. Papoutsi Z, Zhao C, Putnik M, Gustafsson JA, Dahlman-Wright K 2009 Binding of estrogen receptor α/β heterodimers to chromatin in MCF-7 cells. J Mol Endocrinol 43:65-72
41. Tamrazi A, Carlson KE, Daniels JR, Hurth KM, Katzenellenbogen JA 2002 Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol Endocrinol 16:2706-2719
42. Tamrazi A, Carlson KE, Katzenellenbogen JA 2003 Molecular sensors of estrogen receptor conformations and dynamics. Mol Endocrinol 17:2593-2602
43. Hurth KM, Nilges MJ, Carlson KE, Tamrazi A, Belford RL, Katzenellenbogen JA 2004 Ligand-induced changes in estrogen receptor conformation as measured by site-directed spin labeling. Biochemistry 43:1891-1907
44. Kim SH, Tamrazi A, Carlson KE, Katzenellenbogen JA 2005 A proteomic microarray approach for exploring ligand-initiated nuclear hormone receptor pharmacology, receptor selectivity, and heterodimer functionality. Mol Cell Proteomics 4:267-277
45. Manas ES, Unwalla RJ, Xu ZB, Malamas MS, Miller CP, Harris HA, Hsiao C, Akopian T, Hum WT, Malakian K, Wolfrom S, Bapat A, Bhat RA, Stahl ML, Somers WS, Alvarez JC 2004 Structure-based design of estrogen receptor-β selective ligands. J Am Chem Soc 126:15106-15119
46. Tremblay GB, Tremblay A, Labrie F, Giguère V 1999 Dominant activity of activation function 1 (AF-1) and differential stoichiometric requirements for AF-1 and -2 in the estrogen receptor α-β heterodimeric complex. Mol Cell Biol 19:1919-1927
47. El-Tanani M, Fernig DG, Barraclough R, Green C, Rudland P 2001 Differential modulation of transcriptional activity of estrogen receptors by direct protein-protein interactions with the T cell factor family of transcription factors. J Biol Chem 276:41675-41682
48. Shirley SH, Rundhaug JE, Tian J, Cullinan-Ammann N, Lambertz I, Conti CJ, Fuchs-Young R 2009 Transcriptional regulation of estrogen receptor-α by p53 in human breast cancer cells. Cancer Res 69:3405-3414
49. Barnett DH, Sheng S, Charn TH, Waheed A, Sly WS, Lin CY, Liu ET, Katzenellenbogen BS 2008 Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res 68:3505-3515
50. Choi I, Ko C, Park-Sarge OK, Nie R, Hess RA, Graves C, Katzenellenbogen BS 2001 Human estrogen receptor β-specific monoclonal antibodies: characterization and use in studies of estrogen receptor β protein expression in reproductive tissues. Mol Cell Endocrinol 181:139-150
51. Ogawa S, Lozach J, Benner C, Pascual G, Tangirala RK, Westin S, Hoffmann A, Subramaniam S, David M, Rosenfeld MG, Glass CK 2005 Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 122:707-721
52. Matys V, Fricke E, Geffers R, Gössling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Münch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E 2003 TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31:374-378