FOXA1 repression is associated with loss of BRCA1 and increased promoter methylation and chromatin silencing in breast cancer

Oncogene

Volumn 34, Issue 39, 2015, Pages 5012-5024

  Gong, C ^a,b   Fujino, K ^a,c   Monteiro, L J ^a   Gomes, A R ^a   Drost, R ^d   Davidson Smith, H ^e   Takeda, S ^c   Khoo, U S ^b   Jonkers, J ^d   Sproul, D ^e   Lam, E W F ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c JUNTENDO UNIVERSITY   (Japan)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HISTONE; HISTONE H3K27ME3; MESSENGER RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; CHROMATIN; DNA (CYTOSINE 5) METHYLTRANSFERASE; EZH2 PROTEIN, HUMAN; FOXA1 PROTEIN, HUMAN; POLYCOMB REPRESSIVE COMPLEX 2;

ANIMAL CELL; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; BREAST EPITHELIUM CELL; CANCER SURVIVAL; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; EPITHELIAL CANCER CELL LINE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA ANALYSIS; RNA INTERFERENCE; ANIMAL; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GENES, BRCA1; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; MICE; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC;

EID: 84942837100     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.421     Document Type: Article

References (47)

1. Mullan PB, Quinn JE, Harkin DP. The role of BRCA1 in transcriptional regulation and cell cycle control. Oncogene 2006; 25: 5854-5863.
2. Buckley NE, Nic An tSaoir CB, Blayney JK, Oram LC, Crawford NT, D'Costa ZC et al. BRCA1 is a key regulator of breast differentiation through activation of Notch signalling with implications for anti-endocrine treatment of breast cancers. Nucleic Acids Res 2013; 41: 8601-8614.
3. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD et al. BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci USA 2008; 105: 1680-1685.
4. Turner NC, Reis-Filho JS. Basal-like breast cancer and the BRCA1 phenotype. Oncogene 2006; 25: 5846-5853.
5. Hosey AM, Gorski JJ, Murray MM, Quinn JE, Chung WY, Stewart GE et al. Molecular basis for estrogen receptor alpha deficiency in BRCA1-linked breast cancer. J Natl Cancer Inst 2007; 99: 1683-1694.
6. Tkocz D, Crawford NT, Buckley NE, Berry FB, Kennedy RD, Gorski JJ et al. BRCA1 and GATA3 corepress FOXC1 to inhibit the pathogenesis of basal-like breast cancers. Oncogene 2012; 31: 3667-3678.
7. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 2002; 9: 279-289.
8. Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS. Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev 2009; 23: 804-809.
9. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005; 122: 33-43.
10. Mehta RJ, Jain RK, Leung S, Choo J, Nielsen T, Huntsman D et al. FOXA1 is an independent prognostic marker for ER-positive breast cancer. Breast Cancer Res Treat 2012; 131: 881-890.
11. Nakshatri H, Badve S. FOXA1 in breast cancer. Expert Rev Mol Med 2009; 11: e8.
12. Habashy HO, Powe DG, Rakha EA, Ball G, Paish C, Gee J et al. Forkhead-box A1 (FOXA1) expression in breast cancer and its prognostic significance. Eur J Cancer 2008; 44: 1541-1551.
13. Bernardo GM, Bebek G, Ginther CL, Sizemore ST, Lozada KL, Miedler JD et al. FOXA1 represses the molecular phenotype of basal breast cancer cells. Oncogene 2013; 32: 554-563.
14. Nakshatri H, Badve S. FOXA1 as a therapeutic target for breast cancer. Expert Opin Ther Targets 2007; 11: 507-514.
15. Chase A, Cross NC. Aberrations of EZH2 in cancer. Clin Cancer Res 2011; 17: 2613-2618.
16. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-874.
17. Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep 2011; 12: 647-656.
18. Puppe J, Drost R, Liu X, Joosse SA, Evers B, Cornelissen-Steijger P et al. BRCA1- deficient mammary tumor cells are dependent on EZH2 expression and sensitive to polycomb repressive complex 2-inhibitor 3-deazaneplanocin A. Breast cancer Res 2009; 11: R63.
19. Gonzalez ME, DuPrie ML, Krueger H, Merajver SD, Ventura AC, Toy KA et al. Histone methyltransferase EZH2 induces Akt-dependent genomic instability and BRCA1 inhibition in breast cancer. Cancer Res 2011; 71: 2360-2370.
20. Wang L, Zeng X, Chen S, Ding L, Zhong J, Zhao JC et al. BRCA1 is a negative modulator of the PRC2 complex. EMBO J 2013; 32: 1584-1597.
21. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121: 2750-2767.
22. Ehrlich M, Lacey M. DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. Epigenomics 2013; 5: 553-568.
23. Flanagan JM, Cocciardi S, Waddell N, Johnstone CN, Marsh A, Henderson S et al. DNA methylome of familial breast cancer identifies distinct profiles defined by mutation status. Am J Hum Genet 2010; 86: 420-433.
24. Christman JK. 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 2002; 21: 5483-5495.
25. Wu L, Wang F, Xu R, Zhang S, Peng X, Feng Y et al. Promoter methylation of BRCA1 in the prognosis of breast cancer: a meta-analysis. Breast Cancer Res Treat 2013; 142: 619-627.
26. Hsu NC, Huang YF, Yokoyama KK, Chu PY, Chen FM, Hou MF. Methylation of BRCA1 promoter region is associated with unfavorable prognosis in women with early-stage breast cancer. PLoS ONE 2013; 8: e56256.
27. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012; 492: 108-112.
28. Velichutina I, Shaknovich R, Geng H, Johnson NA, Gascoyne RD, Melnick AM et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood 2010; 116: 5247-5255.
29. Hon GC, Hawkins RD, Caballero OL, Lo C, Lister R, Pelizzola M et al. Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res 2012; 22: 246-258.
30. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 2004; 4: 665-676.
31. Albergaria A, Paredes J, Sousa B, Milanezi F, Carneiro V, Bastos J et al. Expression of FOXA1 and GATA-3 in breast cancer: the prognostic significance in hormone receptor-negative tumours. Breast Cancer Res 2009; 11: R40.
32. Novak P, Jensen TJ, Garbe JC, Stampfer MR, Futscher BW. Stepwise DNA methylation changes are linked to escape from defined proliferation barriers and mammary epithelial cell immortalization. Cancer Res 2009; 69: 5251-5258.
33. Reddington JP, Perricone SM, Nestor CE, Reichmann J, Youngson NA, Suzuki M et al. Redistribution of H3K27me3 upon DNA hypomethylation results in derepression of Polycomb target genes. Genome Biol 2013; 14: R25.
34. Li J, Hart RP, Mallimo EM, Swerdel MR, Kusnecov AW, Herrup K. EZH2-mediated H3K27 trimethylation mediates neurodegeneration in ataxia-telangiectasia. Nat Neurosci 2013; 16: 1745-1753.
35. Bae WK, Hennighausen L. Canonical and non-canonical roles of the histone methyltransferase EZH2 in mammary development and cancer. Mol Cell Endocrinol 2014; 382: 593-597.
36. Liu Z, Ren G, Shangguan C, Guo L, Dong Z, Li Y et al. ATRA inhibits the proliferation of DU145 prostate cancer cells through reducing the methylation level of HOXB13 gene. PLoS One 2012; 7: e40943.
37. Martins-Taylor K, Schroeder DI, LaSalle JM, Lalande M, Xu RH. Role of DNMT3B in the regulation of early neural and neural crest specifiers. Epigenetics 2012; 7: 71-82.
38. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 2006; 20: 1123-1136.
39. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007; 128: 735-745.
40. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006; 125: 301-313.
41. Kong SL, Li G, Loh SL, Sung WK, Liu ET. Cellular reprogramming by the conjoint action of ERalpha, FOXA1, and GATA3 to a ligand-inducible growth state. Mol Syst Biol 2011; 7: 526.
42. Bernardo GM, Lozada KL, Miedler JD, Harburg G, Hewitt SC, Mosley JD et al. FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development 2010; 137: 2045-2054.
43. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006; 127: 1041-1055.
44. Wilson BJ, Giguere V. Meta-analysis of human cancer microarrays reveals GATA3 is integral to the estrogen receptor alpha pathway. Mol Cancer 2008; 7: 49.
45. Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M. Positive crossregulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res 2007; 67: 6477-6483.
46. Myatt SS, Kongsema M, Man CW, Kelly DJ, Gomes AR, Khongkow P et al. SUMOylation inhibits FOXM1 activity and delays mitotic transition. Oncogene 2014; 33: 4316-4329.
47. Collado M, Medema RH, Garcia-Cao I, Dubuisson ML, Barradas M, Glassford J et al. Inhibition of the phosphoinositide 3-kinase pathway induces a senescence-like arrest mediated by p27Kip1. J Biol Chem 2000; 275: 21960-21968.