1,052
Views
0
CrossRef citations to date
0
Altmetric
Review

Epigenetic mechanisms of breast cancer: an update of the current knowledge

, , , , , , & show all
Pages 651-664 | Published online: 22 Dec 2014

References

  • Dworkin AM , HuangTH , TolandAE . Epigenetic alterations in the breast: implications for breast cancer detection, prognosis and treatment . Semin. Cancer Biol.19 ( 3 ), 165 – 171 ( 2009 ).
  • Cortez CC , JonesPA . Chromatin, cancer and drug therapies . Mutat. Res.647 ( 1–2 ), 44 – 51 ( 2008 ).
  • Khan SI , AumsuwanP , KhanIA , WalkerLA , DasmahapatraAK . Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome . Chem. Res. Toxicol.25 ( 1 ), 61 – 73 ( 2012 ).
  • Siegel R , NaishadhamD , JemalA . Cancer statistics, 2013 . CA Cancer J. Clin.63 ( 1 ), 11 – 30 ( 2013 ).
  • Dagdemir A , DurifJ , NgolloM , BignonYJ , Bernard-GallonD . Histone lysine trimethylation or acetylation can be modulated by phytoestrogen, estrogen or anti-HDAC in breast cancer cell lines . Epigenomics5 ( 1 ), 51 – 63 ( 2013 ).
  • Esteller M , CornPG , BaylinSB , HermanJG . A gene hypermethylation profile of human cancer . Cancer Res.61 ( 8 ), 3225 – 3229 ( 2001 ).
  • Suzuki J , ChenYY , ScottGKet al. Protein acetylation and histone deacetylase expression associated with malignant breast cancer progression . Clin. Cancer Res.15 ( 9 ), 3163 – 3171 ( 2009 ).
  • Lo PK , SukumarS . Epigenomics and breast cancer . Pharmacogenomics9 ( 12 ), 1879 – 1902 ( 2008 ).
  • Veeck J , EstellerM . Breast cancer epigenetics: From DNA methylation to microRNAs . J. Mammary Gland Biol. Neoplasia15 ( 1 ), 5 – 17 ( 2010 ).
  • Herceg Z , VaissiereT . Epigenetic mechanisms and cancer: an interface between the environment and the genome . Epigenetics6 ( 7 ), 804 – 819 ( 2011 ).
  • Okano M , XieS , LiE . Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells . Nucleic Acids Res.26 ( 11 ), 2536 – 2540 ( 1998 ).
  • Okano M , BellDW , HaberDA , LiE . DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development . Cell99 ( 3 ), 247 – 257 ( 1999 ).
  • Bird A . DNA methylation patterns and epigenetic memory . Genes Dev.16 ( 1 ), 6 – 21 ( 2002 ).
  • Wajed SA , LairdPW , DemeesterTR . DNA methylation: an alternative pathway to cancer . Ann. Surg.234 ( 1 ), 10 – 20 ( 2001 ).
  • Costa FF , VerbisckNV , SalimACet al. Epigenetic silencing of the adhesion molecule ADAM23 is highly frequent in breast tumors . Oncogene23 ( 7 ), 1481 – 1488 ( 2004 ).
  • Oshiro MM , KimCJ , WozniakRJet al. Epigenetic silencing of DSC3 is a common event in human breast cancer . Breast Cancer Res.7 ( 5 ), R669 – 680 ( 2005 ).
  • Holm K , HegardtC , StaafJet al. Molecular subtypes of breast cancer are associated with characteristic DNA methylation patterns . Breast Cancer Res.12 ( 3 ), R36 ( 2010 ).
  • Suzuki H , ToyotaM , CarrawayHet al. Frequent epigenetic inactivation of Wnt antagonist genes in breast cancer . Br. J. Cancer98 ( 6 ), 1147 – 1156 ( 2008 ).
  • Veeck J , NiederacherD , AnHet al. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis . Oncogene25 ( 24 ), 3479 – 3488 ( 2006 ).
  • Veeck J , NoetzelE , BektasNet al. Promoter hypermethylation of the SFRP2 gene is a high-frequent alteration and tumor-specific epigenetic marker in human breast cancer . Mol. Cancer7 , 83 ( 2008 ).
  • Alvarez C , TapiaT , CornejoVet al. Silencing of tumor suppressor genes RASSF1A, SLIT2, and WIF1 by promoter hypermethylation in hereditary breast cancer . Mol. Carcinog.52 ( 6 ), 475 – 487 ( 2013 ).
  • Kajabova V , SmolkovaB , ZmetakovaIet al. RASSF1A promoter methylation levels positively correlate with estrogen receptor expression in breast cancer patients . Transl. Oncol.6 ( 3 ), 297 – 304 ( 2013 ).
  • Li Y , WeiQ , CaoF , CaoX . Expression and promoter methylation of the RASSF1A gene in sporadic breast cancers in Chinese women . Oncol. Rep.19 ( 5 ), 1149 – 1153 ( 2008 ).
  • Xu J , ShettyPB , FengWet al. Methylation of HIN-1, RASSF1A, RIL and CDH13 in breast cancer is associated with clinical characteristics, but only RASSF1A methylation is associated with outcome . BMC Cancer12 , 243 ( 2012 ).
  • Li L , LeeKM , HanWet al. Estrogen and progesterone receptor status affect genome-wide DNA methylation profile in breast cancer . Hum. Mol. Genet.19 ( 21 ), 4273 – 4277 ( 2010 ).
  • Fackler MJ , UmbrichtCB , WilliamsDet al. Genome-wide methylation analysis identifies genes specific to breast cancer hormone receptor status and risk of recurrence . Cancer Res.71 ( 19 ), 6195 – 6207 ( 2011 ).
  • Fang F , TurcanS , RimnerAet al. Breast cancer methylomes establish an epigenomic foundation for metastasis . Sci. Transl. Med.3 ( 75 ), 75ra25 ( 2011 ).
  • Hill VK , RickettsC , BiecheIet al. Genome-wide DNA methylation profiling of CpG islands in breast cancer identifies novel genes associated with tumorigenicity . Cancer Res.71 ( 8 ), 2988 – 2999 ( 2011 ).
  • Guerrero-Preston R , HadarT , OstrowKLet al. Differential promoter methylation of kinesin family member 1a in plasma is associated with breast cancer and DNA repair capacity . Oncol. Rep.32 ( 2 ), 505 – 512 ( 2014 ).
  • Han LL , HouL , ZhouMJet al. Aberrant NDRG1 methylation associated with its decreased expression and clinicopathological significance in breast cancer . J. Biomed. Sci.20 , 52 ( 2013 ).
  • Ramos EA , GrochoskiM , Braun-PradoKet al. Epigenetic changes of CXCR4 and its ligand CXCL12 as prognostic factors for sporadic breast cancer . PLoS ONE6 ( 12 ), e29461 ( 2011 ).
  • Deaton AM , BirdA . CpG islands and the regulation of transcription . Genes Dev.25 ( 10 ), 1010 – 1022 ( 2011 ).
  • Li Y , LiS , ChenJet al. Comparative epigenetic analyses reveal distinct patterns of oncogenic pathways activation in breast cancer subtypes . Hum. Mol. Genet.23 ( 20 ), 5378 – 5393 ( 2014 ).
  • Lindqvist BM , FarkasSA , WingrenS , NilssonTK . DNA methylation pattern of the SLC25A43 gene in breast cancer . Epigenetics7 ( 3 ), 300 – 306 ( 2012 ).
  • Rao X , EvansJ , ChaeHet al. CpG island shore methylation regulates caveolin-1 expression in breast cancer . Oncogene32 ( 38 ), 4519 – 4528 ( 2013 ).
  • Dagdemir A , DurifJ , NgolloM , BignonYJ , Bernard-GallonD . Breast cancer: mechanisms involved in action of phytoestrogens and epigenetic changes . In Vivo27 ( 1 ), 1 – 9 ( 2013 ).
  • Flanagan JM , CocciardiS , WaddellNet al. DNA methylome of familial breast cancer identifies distinct profiles defined by mutation status . Am. J. Hum. Genet.86 ( 3 ), 420 – 433 ( 2010 ).
  • Ruike Y , ImanakaY , SatoF , ShimizuK , TsujimotoG . Genome-wide analysis of aberrant methylation in human breast cancer cells using methyl-DNA immunoprecipitation combined with high-throughput sequencing . BMC Genomics11 , 137 ( 2010 ).
  • Paredes J , AlbergariaA , OliveiraJT , JeronimoC , MilaneziF , SchmittFC . P-cadherin overexpression is an indicator of clinical outcome in invasive breast carcinomas and is associated with CDH3 promoter hypomethylation . Clin. Cancer Res.11 ( 16 ), 5869 – 5877 ( 2005 ).
  • Singh P , YangM , DaiHet al. Overexpression and hypomethylation of flap endonuclease 1 gene in breast and other cancers . Mol. Cancer. Res.6 ( 11 ), 1710 – 1717 ( 2008 ).
  • Kim SJ , KangHS , ChangHLet al. Promoter hypomethylation of the N-acetyltransferase 1 gene in breast cancer . Oncol. Rep.19 ( 3 ), 663 – 668 ( 2008 ).
  • Kristensen LS , NielsenHM , HansenLL . Epigenetics and cancer treatment . Eur. J. Pharmacol.625 ( 1–3 ), 131 – 142 ( 2009 ).
  • Albert M , HelinK . Histone methyltransferases in cancer . Semin. Cell Dev. Biol.21 ( 2 ), 209 – 220 ( 2010 ).
  • Hublitz P , AlbertM , PetersAH . Mechanisms of transcriptional repression by histone lysine methylation . Int. J. Dev. Biol.53 ( 2–3 ), 335 – 354 ( 2009 ).
  • Martin C , ZhangY . The diverse functions of histone lysine methylation . Nat. Rev. Mol. Cell Biol.6 ( 11 ), 838 – 849 ( 2005 ).
  • Elsheikh SE , GreenAR , RakhaEAet al. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome . Cancer Res.69 ( 9 ), 3802 – 3809 ( 2009 ).
  • Guendel I , CarpioL , PedatiCet al. Methylation of the tumor suppressor protein, BRCA1, influences its transcriptional cofactor function . PLoS ONE5 ( 6 ), e11379 ( 2010 ).
  • Choe MK , HongCP , ParkJ , SeoSH , RohTY . Functional elements demarcated by histone modifications in breast cancer cells . Biochem. Biophys. Res. Commun.418 ( 3 ), 475 – 482 ( 2012 ).
  • Hong CP , ChoeMK , RohTY . Characterization of chromatin structure-associated histone modifications in breast cancer cells . Genomics Inform.10 ( 3 ), 145 – 152 ( 2012 ).
  • Hervouet E , CartronPF , JouvenotM , Delage-MourrouxR . Epigenetic regulation of estrogen signaling in breast cancer . Epigenetics8 ( 3 ), 237 – 245 ( 2013 ).
  • Ottaviano YL , IssaJP , ParlFF , SmithHS , BaylinSB , DavidsonNE . Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells . Cancer Res.54 ( 10 ), 2552 – 2555 ( 1994 ).
  • Sharma D , BlumJ , YangX , BeaulieuN , MacleodAR , DavidsonNE . Release of methyl CpG binding proteins and histone deacetylase 1 from the Estrogen receptor alpha (ER) promoter upon reactivation in ER-negative human breast cancer cells . Mol. Endocrinol.19 ( 7 ), 1740 – 1751 ( 2005 ).
  • Ramos EA , CamargoAA , BraunKet al. Simultaneous CXCL12 and ESR1 CpG island hypermethylation correlates with poor prognosis in sporadic breast cancer . BMC Cancer10 , 23 ( 2010 ).
  • Wei M , GrushkoTA , DignamJet al. BRCA1 promoter methylation in sporadic breast cancer is associated with reduced BRCA1 copy number and chromosome 17 aneusomy . Cancer Res.65 ( 23 ), 10692 – 10699 ( 2005 ).
  • Prabhu JS , WahiK , KorlimarlaAet al. The epigenetic silencing of the estrogen receptor (ER) by hypermethylation of the ESR1 promoter is seen predominantly in triple-negative breast cancers in Indian women . Tumour Biol.33 ( 2 ), 315 – 323 ( 2012 ).
  • Zhao L , YuZ , LiYet al. Clinical implications of ERbeta methylation on sporadic breast cancers in Chinese women . Med. Oncol.29 ( 3 ), 1569 – 1575 ( 2012 ).
  • Shen X , LiuY , HsuYJet al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency . Mol. Cell32 ( 4 ), 491 – 502 ( 2008 ).
  • Kleer CG , CaoQ , VaramballySet al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells . Proc. Natl Acad. Sci. USA100 ( 20 ), 11606 – 11611 ( 2003 ).
  • Ding L , ErdmannC , ChinnaiyanAM , MerajverSD , KleerCG . Identification of EZH2 as a molecular marker for a precancerous state in morphologically normal breast tissues . Cancer Res.66 ( 8 ), 4095 – 4099 ( 2006 ).
  • Doherty LF , BromerJG , ZhouY , AldadTS , TaylorHS . In utero exposure to diethylstilbestrol (DES) or bisphenol-A (BPA) increases EZH2 expression in the mammary gland: an epigenetic mechanism linking endocrine disruptors to breast cancer . Horm. Cancer1 ( 3 ), 146 – 155 ( 2010 ).
  • Pal B , BourasT , ShiWet al. Global changes in the mammary epigenome are induced by hormonal cues and coordinated by Ezh2 . Cell Rep.3 ( 2 ), 411 – 426 ( 2013 ).
  • Holm K , GrabauD , LovgrenKet al. Global H3K27 trimethylation and EZH2 abundance in breast tumor subtypes . Mol. Oncol.6 ( 5 ), 494 – 506 ( 2012 ).
  • Ito K , LimAC , Salto-TellezMet al. RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis . Cancer Cell14 ( 3 ), 226 – 237 ( 2008 ).
  • Fujii S , ItoK , ItoY , OchiaiA . Enhancer of zeste homologue 2 (EZH2) down-regulates RUNX3 by increasing histone H3 methylation . J. Biol. Chem.283 ( 25 ), 17324 – 17332 ( 2008 ).
  • Chi XZ , YangJO , LeeKYet al. RUNX3 suppresses gastric epithelial cell growth by inducing p21(WAF1/Cip1) expression in cooperation with transforming growth factor {beta}-activated SMAD . Mol. Cell. Biol.25 ( 18 ), 8097 – 8107 ( 2005 ).
  • Du J , LiL , OuZet al. FOXC1, a target of polycomb, inhibits metastasis of breast cancer cells . Breast Cancer Res. Treat.131 ( 1 ), 65 – 73 ( 2012 ).
  • Yoo KH , HennighausenL . EZH2 methyltransferase and H3K27 methylation in breast cancer . Int. J. Biol. Sci.8 ( 1 ), 59 – 65 ( 2012 ).
  • Matros E , WangZC , LodeiroG , MironA , IglehartJD , RichardsonAL . BRCA1 promoter methylation in sporadic breast tumors: relationship to gene expression profiles . Breast Cancer Res. Treat.91 ( 2 ), 179 – 186 ( 2005 ).
  • Dobrovic A , SimpfendorferD . Methylation of the BRCA1 gene in sporadic breast cancer . Cancer Res.57 ( 16 ), 3347 – 3350 ( 1997 ).
  • Rice JC , OzcelikH , MaxeinerP , AndrulisI , FutscherBW . Methylation of the BRCA1 promoter is associated with decreased BRCA1 mRNA levels in clinical breast cancer specimens . Carcinogenesis21 ( 9 ), 1761 – 1765 ( 2000 ).
  • Esteller M , SilvaJM , DominguezGet al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors . J. Natl Cancer Inst.92 ( 7 ), 564 – 569 ( 2000 ).
  • Turner NC , Reis-FilhoJS , RussellAMet al. BRCA1 dysfunction in sporadic basal-like breast cancer . Oncogene26 ( 14 ), 2126 – 2132 ( 2007 ).
  • Stefansson OA , JonassonJG , OlafsdottirKet al. CpG island hypermethylation of BRCA1 and loss of pRb as co-occurring events in basal/triple-negative breast cancer . Epigenetics6 ( 5 ), 638 – 649 ( 2011 ).
  • Wong EM , SoutheyMC , FoxSBet al. Constitutional methylation of the BRCA1 promoter is specifically associated with BRCA1 mutation-associated pathology in early-onset breast cancer . Cancer Prev. Res.4 ( 1 ), 23 – 33 ( 2011 ).
  • Jung EJ , KimIS , LeeEYet al. Comparison of methylation profiling in cancerous and their corresponding normal tissues from korean patients with breast cancer . Ann. Lab. Med.33 ( 6 ), 431 – 440 ( 2013 ).
  • Iwamoto T , YamamotoN , TaguchiT , TamakiY , NoguchiS . BRCA1 promoter methylation in peripheral blood cells is associated with increased risk of breast cancer with BRCA1 promoter methylation . Breast Cancer Res. Treat.129 ( 1 ), 69 – 77 ( 2011 ).
  • Al-Moghrabi N , Al-QasemAJ , AboussekhraA . Methylation-related mutations in the BRCA1 promoter in peripheral blood cells from cancer-free women . Int. J. Oncol.39 ( 1 ), 129 – 135 ( 2011 ).
  • Sturgeon SR , BalasubramanianR , SchairerC , MussHB , ZieglerRG , ArcaroKF . Detection of promoter methylation of tumor suppressor genes in serum DNA of breast cancer cases and benign breast disease controls . Epigenetics7 ( 11 ), 1258 – 1267 ( 2012 ).
  • Bosviel R , GarciaS , LavediauxGet al. BRCA1 promoter methylation in peripheral blood DNA was identified in sporadic breast cancer and controls . Cancer Epidemiol.36 ( 3 ), e177 – e182 ( 2012 ).
  • Bosviel R , DurifJ , GuoJet al. BRCA2 promoter hypermethylation in sporadic breast cancer . Omics16 ( 12 ), 707 – 710 ( 2012 ).
  • Gonzalez ME , DuprieML , KruegerHet al. Histone methyltransferase EZH2 induces Akt-dependent genomic instability and BRCA1 inhibition in breast cancer . Cancer Res.71 ( 6 ), 2360 – 2370 ( 2011 ).
  • Wang L , HuangH . EZH2 takes the stage when BRCA1 loses . Cell Cycle12 ( 23 ), 3575 – 3576 ( 2013 ).
  • Ververis K , HiongA , KaragiannisTC , LicciardiPV . Histone deacetylase inhibitors (HDACIs): multitargeted anticancer agents . Biologics7 , 47 – 60 ( 2013 ).
  • Mann BS , JohnsonJR , CohenMH , JusticeR , PazdurR . FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma . Oncologist12 ( 10 ), 1247 – 1252 ( 2007 ).
  • Campas-Moya C . Romidepsin for the treatment of cutaneous T-cell lymphoma . Drugs Today45 ( 11 ), 787 – 795 ( 2009 ).
  • Huang L , PardeeAB . Suberoylanilide hydroxamic acid as a potential therapeutic agent for human breast cancer treatment . Mol. Med.6 ( 10 ), 849 – 866 ( 2000 ).
  • Zhou Q , ShawPG , DavidsonNE . Inhibition of histone deacetylase suppresses EGF signaling pathways by destabilizing EGFR mRNA in ER-negative human breast cancer cells . Breast Cancer Res. Treat.117 ( 2 ), 443 – 451 ( 2009 ).
  • Lauricella M , CiraoloA , CarlisiD , VentoR , TesoriereG . SAHA/TRAIL combination induces detachment and anoikis of MDA-MB231 and MCF-7 breast cancer cells . Biochimie94 ( 2 ), 287 – 299 ( 2012 ).
  • Munster PN , ThurnKT , ThomasSet al. A phase II study of the histone deacetylase inhibitor vorinostat combined with tamoxifen for the treatment of patients with hormone therapy-resistant breast cancer . Br. J. Cancer104 ( 12 ), 1828 – 1835 ( 2011 ).
  • Ramaswamy B , FiskusW , CohenBet al. Phase I-II study of vorinostat plus paclitaxel and bevacizumab in metastatic breast cancer: evidence for vorinostat-induced tubulin acetylation and Hsp90 inhibition in vivo . Breast Cancer Res. Treat.132 ( 3 ), 1063 – 1072 ( 2012 ).
  • Tate CR , RhodesLV , SegarHCet al. Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat . Breast Cancer Res.14 ( 3 ), R79 ( 2012 ).
  • Nohara K , YokoyamaY , KanoK . The important role of caspase-10 in sodium butyrate-induced apoptosis . Kobe J. Med. Sci.53 ( 5 ), 265 – 273 ( 2007 ).
  • Cho HJ , KimSY , KimKHet al. The combination effect of sodium butyrate and 5-Aza-2’-deoxycytidine on radiosensitivity in RKO colorectal cancer and MCF-7 breast cancer cell lines . World J. Surg. Oncol.7 , 49 ( 2009 ).
  • Sharma D , SaxenaNK , DavidsonNE , VertinoPM . Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes . Cancer Res.66 ( 12 ), 6370 – 6378 ( 2006 ).
  • Fan J , YinWJ , LuJSet al. ER alpha negative breast cancer cells restore response to endocrine therapy by combination treatment with both HDAC inhibitor and DNMT inhibitor . J. Cancer Res. Clin. Oncol.134 ( 8 ), 883 – 890 ( 2008 ).
  • Yang X , PhillipsDL , FergusonAT , NelsonWG , HermanJG , DavidsonNE . Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells . Cancer Res.61 ( 19 ), 7025 – 7029 ( 2001 ).
  • Sabnis GJ , GoloubevaO , ChumsriS , NguyenN , SukumarS , BrodieAM . Functional activation of the estrogen receptor-alpha and aromatase by the HDAC inhibitor entinostat sensitizes ER-negative tumors to letrozole . Cancer Res.71 ( 5 ), 1893 – 1903 ( 2011 ).
  • Chiang PK , CantoniGL . Perturbation of biochemical transmethylations by 3-deazaadenosine in vivo . Biochem. Pharmacol.28 ( 12 ), 1897 – 1902 ( 1979 ).
  • Liu S , WolfeMS , BorchardtRT . Rational approaches to the design of antiviral agents based on S-adenosyl-L-homocysteine hydrolase as a molecular target . Antiviral Res.19 ( 3 ), 247 – 265 ( 1992 ).
  • Tan J , YangX , ZhuangLet al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells . Genes Dev.21 ( 9 ), 1050 – 1063 ( 2007 ).
  • Toland AE . Aberrant epigenetic regulation in breast cancer (p91-122) . In : Patho-Epigenetics of Disease.MinarovitsJ , NillerHH ( Eds ). Springer , NY, USA ( 2012 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.