Epi-drugs as triple-negative breast cancer treatment

References

• Bray F , FerlayJ , SoerjomataramI , SiegelRL , TorreLA , JemalA. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.68(6), 394–424 (2018).
   PubMed Web of Science ®Google Scholar
• Fragomeni SM , SciallisA , JerussJS. Molecular subtypes and local-regional control of breast cancer. Surg. Oncol. Clin. N. Am.27(1), 95–120 (2018).
   PubMed Web of Science ®Google Scholar
• Temian DC , PopLA , IrimieAI , Berindan-NeagoeI. The epigenetics of triple-negative and basal-like breast cancer: current knowledge. J. Breast Cancer21(3), 233–243 (2018).
   PubMed Web of Science ®Google Scholar
• Huang Y , NayakS , JankowitzR , DavidsonNE , OesterreichS. Epigenetics in breast cancer: what’s new?Breast Cancer Res.13(6), 225 (2011).
   PubMed Web of Science ®Google Scholar
• Nebbioso A , CarafaV , BenedettiR , AltucciL. Trials with ‘epigenetic’ drugs: an update. Mol. Oncol.6(6), 657–682 (2012).
   PubMed Web of Science ®Google Scholar
• Nebbioso A , TambaroFP , Dell’aversanaC , AltucciL. Cancer epigenetics: moving forward. PLoS Genet.14(6), e1007362 (2018).
   PubMed Web of Science ®Google Scholar
• Sigalotti L , FrattaE , CoralS , MaioM. Epigenetic drugs as immunomodulators for combination therapies in solid tumors. Pharmacol. Ther.142(3), 339–350 (2014).
   PubMed Web of Science ®Google Scholar
• Judes G , RifaiK , DauresMet al. High-throughput «Omics» technologies: new tools for the study of triple-negative breast cancer. Cancer Lett.382(1), 77–85 (2016).
   PubMed Web of Science ®Google Scholar
• Raju R , PaulAM , AsokachandranVet al. The Triple-Negative Breast Cancer Database: an omics platform for reference, integration and analysis of triple-negative breast cancer data. Breast Cancer Res.16(6), 490 (2014).
   PubMed Web of Science ®Google Scholar
• Audia JE , CampbellRM. Histone modifications and cancer. Cold Spring Harb. Perspect. Biol.8(4), a019521 (2016).
   PubMed Web of Science ®Google Scholar
• Lustberg MB , RamaswamyB. Epigenetic therapy in breast cancer. Curr. Breast Cancer Rep.3(1), 34–43 (2011).
   PubMedGoogle Scholar
• Subramaniam D , ThombreR , DharA , AnantS. DNA methyltransferases: a novel target for prevention and therapy. Front. Oncol.4, 80 (2014).
   PubMedGoogle Scholar
• Stearns V , ZhouQ , DavidsonNE. Epigenetic regulation as a new target for breast cancer therapy. Cancer Invest.25(8), 659–665 (2007).
   PubMed Web of Science ®Google Scholar
• Pirola L , CiesielskiO , BalcerczykA. The methylation status of the epigenome: its emerging role in the regulation of tumor angiogenesis and tumor growth, and potential for drug targeting. Cancers (Basel)10(8), E268 (2018).
   PubMed Web of Science ®Google Scholar
• Yu J , QinB , MoyerAMet al. DNA methyltransferase expression in triple-negative breast cancer predicts sensitivity to decitabine. J. Clin. Invest.128(6), 2376–2388 (2018).
   PubMed Web of Science ®Google Scholar
• Portela A , EstellerM. Epigenetic modifications and human disease. Nat. Biotechnol.28(10), 1057–1068 (2010).
   PubMed Web of Science ®Google Scholar
• Tsai HC , LiH , Van NesteLet al. Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell21(3), 430–446 (2012).
   PubMed Web of Science ®Google Scholar
• Mirza S , SharmaG , PandyaP , RalhanR. Demethylating agent 5-aza-2-deoxycytidine enhances susceptibility of breast cancer cells to anticancer agents. Mol. Cell. Biochem.342(1–2), 101–109 (2010).
   PubMed Web of Science ®Google Scholar
• Connolly RM , LiH , JankowitzRCet al. Combination epigenetic therapy in advanced breast cancer with 5-azacitidine and entinostat: a Phase II National Cancer Institute/Stand Up to Cancer Study. Clin. Cancer Res.23(11), 2691–2701 (2017).
   PubMed Web of Science ®Google Scholar
• Champion C , Guianvarc’hD , Senamaud-BeaufortCet al. Mechanistic insights on the inhibition of c5 DNA methyltransferases by zebularine. PLoS ONE5(8), e12388 (2010).
   PubMed Web of Science ®Google Scholar
• Nakamura K , AizawaK , NakabayashiKet al. DNA methyltransferase inhibitor zebularine inhibits human hepatic carcinoma cells proliferation and induces apoptosis. PLoS ONE8(1), e54036 (2013).
   PubMed Web of Science ®Google Scholar
• Nakamura K , NakabayashiK , HtetAung Ket al. DNA methyltransferase inhibitor zebularine induces human cholangiocarcinoma cell death through alteration of DNA methylation status. PLoS ONE10(3), e0120545 (2015).
   PubMed Web of Science ®Google Scholar
• Kong WY , YeeZY , MaiCW , FangCM , AbdullahS , NgaiSC. Zebularine and trichostatin A sensitized human breast adenocarcinoma cells towards tumor necrosis factor-related apoptosis inducing ligand (TRAIL)-induced apoptosis. Heliyon5(9), e02468 (2019).
   PubMed Web of Science ®Google Scholar
• Yan L , NassSJ , SmithD , NelsonWG , HermanJG , DavidsonNE. Specific inhibition of DNMT1 by antisense oligonucleotides induces re-expression of estrogen receptor-alpha (ER) in ER-negative human breast cancer cell lines. Cancer Biol. Ther.2(5), 552–556 (2003).
   PubMed Web of Science ®Google Scholar
• Davis AJ , GelmonKA , SiuLLet al. Phase I and pharmacologic study of the human DNA methyltransferase antisense oligodeoxynucleotide MG98 given as a 21-day continuous infusion every 4 weeks. Invest. New Drugs21(1), 85–97 (2003).
   PubMed Web of Science ®Google Scholar
• Stewart DJ , DonehowerRC , EisenhauerEAet al. A Phase I pharmacokinetic and pharmacodynamic study of the DNA methyltransferase 1 inhibitor MG98 administered twice weekly. Ann. Oncol.14(5), 766–774 (2003).
   PubMed Web of Science ®Google Scholar
• Schneeberger Y , StenzigJ , HubnerF , SchaeferA , ReichenspurnerH , EschenhagenT. Pharmacokinetics of the experimental non-nucleosidic DNA methyl transferase inhibitor N-Phthalyl-L-Tryptophan (RG 108) in rats. Basic Clin. Pharmacol. Toxicol.118(5), 327–332 (2016).
   PubMed Web of Science ®Google Scholar
• Braun J , BoittiauxI , TilborgA , LambertD , WoutersJ. The dicyclo-hexyl-amine salt of RG108 (N-phthalyl-l-tryptophan), a potential epigenetic modulator. Acta Crystallogr. Sect. E Struct. Rep. Online66(Pt 12), o3175–o3176 (2010).
   PubMedGoogle Scholar
• Borges S , DopplerHR , StorzP. A combination treatment with DNA methyltransferase inhibitors and suramin decreases invasiveness of breast cancer cells. Breast Cancer Res. Treat.144(1), 79–91 (2014).
   PubMed Web of Science ®Google Scholar
• Lee BH , YegnasubramanianS , LinX , NelsonWG. Procainamide is a specific inhibitor of DNA methyltransferase 1. J. Biol. Chem.280(49), 40749–40756 (2005).
   PubMed Web of Science ®Google Scholar
• Morissette G , MoreauE , CGR , MarceauF. N-substituted 4-aminobenzamides (procainamide analogs): an assessment of multiple cellular effects concerning ion trapping. Mol. Pharmacol.68(6), 1576–1589 (2005).
   PubMed Web of Science ®Google Scholar
• Villar-Garea A , FragaMF , EspadaJ , EstellerM. Procaine is a DNA-demethylating agent with growth-inhibitory effects in human cancer cells. Cancer Res.63(16), 4984–4989 (2003).
   PubMed Web of Science ®Google Scholar
• Lin J , HaffnerMC , ZhangYet al. Disulfiram is a DNA demethylating agent and inhibits prostate cancer cell growth. Prostate71(4), 333–343 (2011).
   PubMed Web of Science ®Google Scholar
• Veverka KA , JohnsonKL , MaysDC , LipskyJJ , NaylorS. Inhibition of aldehyde dehydrogenase by disulfiram and its metabolite methyl diethylthiocarbamoyl-sulfoxide. Biochem. Pharmacol.53(4), 511–518 (1997).
   PubMed Web of Science ®Google Scholar
• Yang Z , GuoF , AlbersAE , SehouliJ , KaufmannAM. Disulfiram modulates ROS accumulation and overcomes synergistically cisplatin resistance in breast cancer cell lines. Biomed. Pharmacother.113, 108727 (2019).
   PubMed Web of Science ®Google Scholar
• Han D , WuG , ChangCet al. Disulfiram inhibits TGF-beta-induced epithelial–mesenchymal transition and stem-like features in breast cancer via ERK/NF-κB/Snail pathway. Oncotarget6(38), 40907–40919 (2015).
   PubMedGoogle Scholar
• Zhang Q , LinZ , YinXet al. In vitro and in vivo study of hydralazine, a potential anti-angiogenic agent. Eur. J. Pharmacol.779, 138–146 (2016).
   PubMed Web of Science ®Google Scholar
• Jiang Y , HuangY , ChengCet al. Combination of thiazolidinedione and hydralazine suppresses proliferation and induces apoptosis by PPARγ up-expression in MDA-MB-231 cells. Exp. Mol. Pathol.91(3), 768–774 (2011).
   PubMed Web of Science ®Google Scholar
• Candelaria M , Gallardo-RinconD , ArceCet al. A Phase II study of epigenetic therapy with hydralazine and magnesium valproate to overcome chemotherapy resistance in refractory solid tumors. Ann. Oncol.18(9), 1529–1538 (2007).
   PubMed Web of Science ®Google Scholar
• Schroder L , MarahrensP , KochJGet al. Effects of green tea, matcha tea and their components epigallocatechin gallate and quercetin on MCF7 and MDA-MB-231 breast carcinoma cells. Oncol. Rep.41(1), 387–396 (2019).
   PubMed Web of Science ®Google Scholar
• Bimonte S , CascellaM , BarbieriA , ArraC , CuomoA. Shining a light on the effects of the combination of (-)-Epigallocatechin-3-gallate and Tapentadol on the growth of human triple-negative breast cancer cells. In Vivo33(5), 1463–1468 (2019).
   PubMed Web of Science ®Google Scholar
• Wei R , MaoL , XuPet al. Suppressing glucose metabolism with epigallocatechin-3-gallate (EGCG) reduces breast cancer cell growth in preclinical models. Food Funct.9(11), 5682–5696 (2018).
   PubMed Web of Science ®Google Scholar
• Zhao H , ZhuW , JiaLet al. Phase I study of topical epigallocatechin-3-gallate (EGCG) in patients with breast cancer receiving adjuvant radiotherapy. Br. J. Radiol.89(1058), 20150665 (2016).
   PubMed Web of Science ®Google Scholar
• Fang M , ChenD , YangCS. Dietary polyphenols may affect DNA methylation. J. Nutr.137(Suppl. 1), S223–S228 (2007).
   Web of Science ®Google Scholar
• Gupta SC , PatchvaS , AggarwalBB. Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J.15(1), 195–218 (2013).
   PubMed Web of Science ®Google Scholar
• Martinez N , HerreraM , FriasLet al. A combination of hydroxytyrosol, omega-3 fatty acids and curcumin improves pain and inflammation among early stage breast cancer patients receiving adjuvant hormonal therapy: results of a pilot study. Clin. Transl. Oncol.21(4), 489–498 (2019).
   PubMed Web of Science ®Google Scholar
• Greer EL , Beese-SimsSE , BrookesEet al. A histone methylation network regulates transgenerational epigenetic memory in C. elegans. Cell Rep.7(1), 113–126 (2014).
   PubMed Web of Science ®Google Scholar
• Michalak EM , VisvaderJE. Dysregulation of histone methyltransferases in breast cancer - opportunities for new targeted therapies? Mol. Oncol.10(10), 1497–1515 (2016).
   PubMed Web of Science ®Google Scholar
• Hervouet E , CartronPF , JouvenotM , Delage-MourrouxR. Epigenetic regulation of estrogen signaling in breast cancer. Epigenetics8(3), 237–245 (2013).
   PubMed Web of Science ®Google Scholar
• Patani N , JiangWG , NewboldRF , MokbelK. Histone-modifier gene expression profiles are associated with pathological and clinical outcomes in human breast cancer. Anticancer Res.31(12), 4115–4125 (2011).
   PubMed Web of Science ®Google Scholar
• Liu L , KimballS , LiuH , HolowatyjA , YangZQ. Genetic alterations of histone lysine methyltransferases and their significance in breast cancer. Oncotarget6(4), 2466–2482 (2015).
   PubMed Web of Science ®Google Scholar
• Lehnertz B , UedaY , DerijckAAet al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol.13(14), 1192–1200 (2003).
   PubMed Web of Science ®Google Scholar
• Yang G , WengX , ZhaoYet al. The histone H3K9 methyltransferase SUV39H links SIRT1 repression to myocardial infarction. Nat. Commun.8, 14941 (2017).
   PubMed Web of Science ®Google Scholar
• Peters AH , O’carrollD , ScherthanHet al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell107(3), 323–337 (2001).
   PubMed Web of Science ®Google Scholar
• Dreger H , LudwigA , WellerAet al. Epigenetic regulation of cell adhesion and communication by enhancer of zeste homolog 2 in human endothelial cells. Hypertension60(5), 1176–1183 (2012).
   PubMed Web of Science ®Google Scholar
• Crea F , FornaroL , BocciGet al. EZH2 inhibition: targeting the crossroad of tumor invasion and angiogenesis. Cancer Metastasis Rev.31(3–4), 753–761 (2012).
   PubMed Web of Science ®Google Scholar
• Ngollo M , LebertA , DagdemirAet al. The association between histone 3 lysine 27 trimethylation (H3K27me3) and prostate cancer: relationship with clinicopathological parameters. BMC Cancer14, 994 (2014).
   PubMed Web of Science ®Google Scholar
• Daures M , IdrissouM , JudesGet al. A new metabolic gene signature in prostate cancer regulated by JMJD3 and EZH2. Oncotarget9(34), 23413–23425 (2018).
   PubMedGoogle Scholar
• Judes G , DagdemirA , Karsli-CeppiogluSet al. H3K4 acetylation, H3K9 acetylation and H3K27 methylation in breast tumor molecular subtypes. Epigenomics8(7), 909–924 (2016).
   PubMed Web of Science ®Google Scholar
• Liu S , YeD , GuoWet al. G9a is essential for EMT-mediated metastasis and maintenance of cancer stem cell-like characters in head and neck squamous cell carcinoma. Oncotarget6(9), 6887–6901 (2015).
   PubMedGoogle Scholar
• Ding J , LiT , WangXet al. The histone H3 methyltransferase G9A epigenetically activates the serine-glycine synthesis pathway to sustain cancer cell survival and proliferation. Cell Metab.18(6), 896–907 (2013).
   PubMed Web of Science ®Google Scholar
• Chen H , YanY , DavidsonTL , ShinkaiY , CostaM. Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells. Cancer Res.66(18), 9009–9016 (2006).
   PubMed Web of Science ®Google Scholar
• Chen MW , HuaKT , KaoHJet al. H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer Res.70(20), 7830–7840 (2010).
   PubMed Web of Science ®Google Scholar
• Lee SH , KimJ , KimWH , LeeYM. Hypoxic silencing of tumor suppressor RUNX3 by histone modification in gastric cancer cells. Oncogene28(2), 184–194 (2009).
   PubMed Web of Science ®Google Scholar
• Wojtala M , Macierzynska-PiotrowskaE , RybaczekD , PirolaL , BalcerczykA. Pharmacological and transcriptional inhibition of the G9a histone methyltransferase suppresses proliferation and modulates redox homeostasis in human microvascular endothelial cells. Pharmacol. Res.128, 252–263 (2018).
   PubMed Web of Science ®Google Scholar
• Duan Y , WuX , ZhaoQet al. DOT1L promotes angiogenesis through cooperative regulation of VEGFR2 with ETS-1. Oncotarget7(43), 69674–69687 (2016).
   PubMedGoogle Scholar
• Zhang Y , LiuJ , LinJet al. The transcription factor GATA1 and the histone methyltransferase SET7 interact to promote VEGF-mediated angiogenesis and tumor growth and predict clinical outcome of breast cancer. Oncotarget7(9), 9859–9875 (2016).
   PubMedGoogle Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Martin-Sanchez E , MendazaS , Ulazia-GarmendiaAet al. CDH22 hypermethylation is an independent prognostic biomarker in breast cancer. Clin. Epigenetics9, 7 (2017).
   PubMed Web of Science ®Google Scholar
• Pan M , ReidMA , LowmanXHet al. Regional glutamine deficiency in tumours promotes dedifferentiation through inhibition of histone demethylation. Nat. Cell. Biol.18(10), 1090–1101 (2016).
   PubMed Web of Science ®Google Scholar
• Greiner D , BonaldiT , EskelandR , RoemerE , ImhofA. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3-9. Nat. Chem. Biol.1(3), 143–145 (2005).
   PubMed Web of Science ®Google Scholar
• 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. Cell.32(4), 491–502 (2008).
   PubMed Web of Science ®Google Scholar
• Karsli-Ceppioglu S , DagdemirA , JudesGet al. Epigenetic mechanisms of breast cancer: an update of the current knowledge. Epigenomics6(6), 651–664 (2014).
   PubMed Web of Science ®Google Scholar
• Dagdemir A , JudesG , LebertAet al. Epigenetic modifications with DZNep, NaBu and SAHA in luminal and mesenchymal-like breast cancer subtype cells. Cancer Genomics Proteomics13(4), 291–303 (2016).
   PubMed Web of Science ®Google Scholar
• Vinet M , SureshS , MaireVet al. Protein arginine methyltransferase 5: a novel therapeutic target for triple-negative breast cancers. Cancer Med.8(5), 2414–2428 (2019).
   PubMed Web of Science ®Google Scholar
• Schulte JH , LimS , SchrammAet al. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res.69(5), 2065–2071 (2009).
   PubMed Web of Science ®Google Scholar
• Harris WJ , HuangX , LynchJTet al. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell21(4), 473–487 (2012).
   PubMed Web of Science ®Google Scholar
• Schenk T , ChenWC , GollnerSet al. Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat. Med.18(4), 605–611 (2012).
   PubMed Web of Science ®Google Scholar
• Wang Y , ZhangH , ChenYet al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell138(4), 660–672 (2009).
   PubMed Web of Science ®Google Scholar
• Huang X , PateromichelakisS , HillsAet al. p53 mutations in deep tissues are more strongly associated with recurrence than mutation-positive mucosal margins. Clin. Cancer Res.13(20), 6099–6106 (2007).
   PubMed Web of Science ®Google Scholar
• Yang Y , YinX , YangH , XuY. Histone demethylase LSD2 acts as an E3 ubiquitin ligase and inhibits cancer cell growth through promoting proteasomal degradation of OGT. Mol. Cell58(1), 47–59 (2015).
   PubMed Web of Science ®Google Scholar
• Lee MG , WynderC , CoochN , ShiekhattarR. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature437(7057), 432–435 (2005).
   PubMed Web of Science ®Google Scholar
• Wagner KW , AlamH , DharSSet al. KDM2A promotes lung tumorigenesis by epigenetically enhancing ERK1/2 signaling. J. Clin. Invest.123(12), 5231–5246 (2013).
   PubMed Web of Science ®Google Scholar
• He J , NguyenAT , ZhangY. KDM2b/JHDM1b, an H3K36me2-specific demethylase, is required for initiation and maintenance of acute myeloid leukemia. Blood117(14), 3869–3880 (2011).
   PubMed Web of Science ®Google Scholar
• Park MH , HongJT. Roles of NF-κB in cancer and inflammatory diseases and their therapeutic approaches. Cells5(2), E15 (2016).
   PubMed Web of Science ®Google Scholar
• Beyer S , KristensenMM , JensenKS , JohansenJV , StallerP. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J. Biol. Chem.283(52), 36542–36552 (2008).
   PubMed Web of Science ®Google Scholar
• Krieg AJ , RankinEB , ChanD , RazorenovaO , FernandezS , GiacciaAJ. Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 α enhances hypoxic gene expression and tumor growth. Mol. Cell. Biol.30(1), 344–353 (2010).
   PubMed Web of Science ®Google Scholar
• Black JC , AtabakhshE , KimJet al. Hypoxia drives transient site-specific copy gain and drug-resistant gene expression. Genes Dev.29(10), 1018–1031 (2015).
   PubMed Web of Science ®Google Scholar
• Black JC , ManningAL , Van RechemCet al. KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumors. Cell154(3), 541–555 (2013).
   PubMed Web of Science ®Google Scholar
• Bertos NR , WangAH , YangXJ. Class II histone deacetylases: structure, function, and regulation. Biochem. Cell Biol.79(3), 243–252 (2001).
   PubMedGoogle Scholar
• Lin W , CaoJ , LiuJet al. Loss of the retinoblastoma binding protein 2 (RBP2) histone demethylase suppresses tumorigenesis in mice lacking Rb1 or Men1. Proc. Natl Acad. Sci. USA108(33), 13379–13386 (2011).
   PubMed Web of Science ®Google Scholar
• Sharma SV , LeeDY , LiBet al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell141(1), 69–80 (2010).
   PubMed Web of Science ®Google Scholar
• Wang GG , SongJ , WangZet al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature459(7248), 847–851 (2009).
   PubMed Web of Science ®Google Scholar
• Huether R , DongL , ChenXet al. The landscape of somatic mutations in epigenetic regulators across 1,000 paediatric cancer genomes. Nat. Commun.5, 3630 (2014).
   PubMed Web of Science ®Google Scholar
• Kandoth C , MclellanMD , VandinFet al. Mutational landscape and significance across 12 major cancer types. Nature502(7471), 333–339 (2013).
   PubMed Web of Science ®Google Scholar
• Svotelis A , BiancoS , MadoreJet al. H3K27 demethylation by JMJD3 at a poised enhancer of anti-apoptotic gene BCL2 determines ERα ligand dependency. EMBO J.30(19), 3947–3961 (2011).
   PubMed Web of Science ®Google Scholar
• Van Haaften G , DalglieshGL , DaviesHet al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat. Genet.41(5), 521–523 (2009).
   PubMed Web of Science ®Google Scholar
• D’oto A , TianQW , DavidoffAM , YangJ. Histone demethylases and their roles in cancer epigenetics. J. Med. Oncol. Ther.1(2), 34–40 (2016).
   PubMedGoogle Scholar
• Kruidenier L , ChungCW , ChengZet al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature488(7411), 404–408 (2012).
   PubMed Web of Science ®Google Scholar
• Hashizume R , AndorN , IharaYet al. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat. Med.20(12), 1394–1396 (2014).
   PubMed Web of Science ®Google Scholar
• Yan N , XuL , WuXet al. GSKJ4, an H3K27me3 demethylase inhibitor, effectively suppresses the breast cancer stem cells. Exp. Cell Res.359(2), 405–414 (2017).
   PubMed Web of Science ®Google Scholar
• Ntziachristos P , TsirigosA , WelsteadGGet al. Contrasting roles of histone 3 lysine 27 demethylases in acute lymphoblastic leukaemia. Nature514(7523), 513–517 (2014).
   PubMed Web of Science ®Google Scholar
• Sakaki H , OkadaM , KuramotoKet al. GSKJ4, a selective Jumonji H3K27 demethylase inhibitor, effectively targets ovarian cancer stem cells. Anticancer Res.35(12), 6607–6614 (2015).
   PubMed Web of Science ®Google Scholar
• Donas C , CarrascoM , FritzMet al. The histone demethylase inhibitor GSK-J4 limits inflammation through the induction of a tolerogenic phenotype on DCs. J. Autoimmun.75, 105–117 (2016).
   PubMed Web of Science ®Google Scholar
• Backe MB , AnderssonJL , BacosKet al. Lysine demethylase inhibition protects pancreatic beta cells from apoptosis and improves β-cell function. Mol. Cell. Endocrinol.460, 47–56 (2018).
   PubMed Web of Science ®Google Scholar
• Messer HG , JacobsD , DhummakuptA , BloomDC. Inhibition of H3K27me3-specific histone demethylases JMJD3 and UTX blocks reactivation of herpes simplex virus 1 in trigeminal ganglion neurons. J. Virol.89(6), 3417–3420 (2015).
   PubMed Web of Science ®Google Scholar
• Schmidt DM , MccaffertyDG. Trans-2-Phenylcyclopropylamine is a mechanism-based inactivator of the histone demethylase LSD1. Biochemistry46(14), 4408–4416 (2007).
   PubMed Web of Science ®Google Scholar
• Ferrari-Amorotti G , ChiodoniC , ShenFet al. Suppression of invasion and metastasis of triple-negative breast cancer lines by pharmacological or genetic inhibition of slug activity. Neoplasia16(12), 1047–1058 (2014).
   PubMed Web of Science ®Google Scholar
• Prusevich P , KalinJH , MingSAet al. A selective phenelzine analogue inhibitor of histone demethylase LSD1. ACS Chem. Biol.9(6), 1284–1293 (2014).
   PubMed Web of Science ®Google Scholar
• Wade PA , PrussD , WolffeAP. Histone acetylation: chromatin in action. Trends Biochem. Sci.22(4), 128–132 (1997).
   PubMed Web of Science ®Google Scholar
• Orr JA , HamiltonPW. Histone acetylation and chromatin pattern in cancer. A review. Anal Quant. Cytol. Histol.29(1), 17–31 (2007).
   PubMedGoogle Scholar
• Marmorstein R , RothSY. Histone acetyltransferases: function, structure, and catalysis. Curr. Opin. Genet. Dev.11(2), 155–161 (2001).
   PubMed Web of Science ®Google Scholar
• Roth SY , DenuJM , AllisCD. Histone acetyltransferases. Annu. Rev. Biochem.70, 81–120 (2001).
   PubMed Web of Science ®Google Scholar
• Avvakumov N , CoteJ. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene26(37), 5395–5407 (2007).
   PubMed Web of Science ®Google Scholar
• Utley RT , CoteJ. The MYST family of histone acetyltransferases. Curr. Top. Microbiol. Immunol.274, 203–236 (2003).
   PubMed Web of Science ®Google Scholar
• Doyon Y , SelleckW , LaneWS , TanS , CoteJ. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell. Biol.24(5), 1884–1896 (2004).
   PubMed Web of Science ®Google Scholar
• Chan HM , LaThangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci.114(Pt 13), 2363–2373 (2001).
   PubMed Web of Science ®Google Scholar
• Bedford DC , KasperLH , FukuyamaT , BrindlePK. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics5(1), 9–15 (2010).
   PubMed Web of Science ®Google Scholar
• Eckner R . p300 and CBP as transcriptional regulators and targets of oncogenic events. Biol. Chem.377(11), 685–688 (1996).
   PubMed Web of Science ®Google Scholar
• Nagy Z , PankotaiT. Histone acetylation gets complicated. Cell Cycle9(13), 2501 (2010).
   PubMed Web of Science ®Google Scholar
• Salah Ud-Din AI , TikhomirovaA , RoujeinikovaA. Structure and functional diversity of GCN5-related N-acetyltransferases (GNAT). Int. J. Mol. Sci.17(7), (2016).
   Web of Science ®Google Scholar
• Gao C , BourkeE , ScobieMet al. Rational design and validation of a Tip60 histone acetyltransferase inhibitor. Sci. Rep.4, 5372 (2014).
   PubMed Web of Science ®Google Scholar
• Idrissou M , JudesG , DauresMet al. TIP60 inhibitor TH1834 reduces breast cancer progression in xenografts in mice. OMICS23(9), 457–459 (2019).
   PubMed Web of Science ®Google Scholar
• Brown JA , BourkeE , ErikssonLA , KerinMJ. Targeting cancer using KAT inhibitors to mimic lethal knockouts. Biochem. Soc. Trans.44(4), 979–986 (2016).
   PubMedGoogle Scholar
• Judes G , DuboisL , RifaiKet al. TIP60: an actor in acetylation of H3K4 and tumor development in breast cancer. Epigenomics10(11), 1415–1430 (2018).
   PubMed Web of Science ®Google Scholar
• Judes G , RifaiK , NgolloMet al. A bivalent role of TIP60 histone acetyl transferase in human cancer. Epigenomics7(8), 1351–1363 (2015).
   PubMed Web of Science ®Google Scholar
• Idrissou M , RifaiK , DauresM , Penault-LlorcaF , BignonYJ , Bernard-GallonD. Exciting history of Tip60 and its companions in carcinogenesis across the heterochromatin landscapes. OMICS22(9), 626–628 (2018).
   PubMed Web of Science ®Google Scholar
• Coffey K , BlackburnTJ , CookSet al. Characterisation of a Tip60 specific inhibitor, NU9056, in prostate cancer. PLoS ONE7(10), e45539 (2012).
   PubMed Web of Science ®Google Scholar
• Balasubramanyam K , AltafM , VarierRAet al. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J. Biol. Chem.279(32), 33716–33726 (2004).
   PubMed Web of Science ®Google Scholar
• Balasubramanyam K , SwaminathanV , RanganathanA , KunduTK. Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem.278(21), 19134–19140 (2003).
   PubMed Web of Science ®Google Scholar
• Gajer JM , FurdasSD , GrunderAet al. Histone acetyltransferase inhibitors block neuroblastoma cell growth in vivo. Oncogenesis4, e137 (2015).
   PubMed Web of Science ®Google Scholar
• Tu SH , ChiouYS , KalyanamN , HoCT , ChenLC , PanMH. Garcinol sensitizes breast cancer cells to Taxol through the suppression of caspase-3/iPLA2 and NF-kappaB/Twist1 signaling pathways in a mouse 4T1 breast tumor model. Food Funct.8(3), 1067–1079 (2017).
   PubMed Web of Science ®Google Scholar
• Moser MA , HagelkruysA , SeiserC. Transcription and beyond: the role of mammalian class I lysine deacetylases. Chromosoma123(1–2), 67–78 (2014).
   PubMed Web of Science ®Google Scholar
• Haberland M , MontgomeryRL , OlsonEN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet.10(1), 32–42 (2009).
   PubMed Web of Science ®Google Scholar
• Lahm A , PaoliniC , PallaoroMet al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl Acad. Sci. USA104(44), 17335–17340 (2007).
   PubMed Web of Science ®Google Scholar
• Di Giorgio E , GagliostroE , BrancoliniC. Selective class IIa HDAC inhibitors: myth or reality. Cell. Mol. Life Sci.72(1), 73–86 (2015).
   PubMed Web of Science ®Google Scholar
• Hubbert C , GuardiolaA , ShaoRet al. HDAC6 is a microtubule-associated deacetylase. Nature417(6887), 455–458 (2002).
   PubMed Web of Science ®Google Scholar
• Gao L , CuetoMA , AsselbergsF , AtadjaP. Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J. Biol. Chem.277(28), 25748–25755 (2002).
   PubMed Web of Science ®Google Scholar
• Bosch-Presegue L , VaqueroA. Sirtuin-dependent epigenetic regulation in the maintenance of genome integrity. FEBS J.282(9), 1745–1767 (2015).
   PubMed Web of Science ®Google Scholar
• Martinez-Redondo P , VaqueroA. The diversity of histone versus nonhistone sirtuin substrates. Genes Cancer4(3–4), 148–163 (2013).
   PubMedGoogle Scholar
• Yuan H , SuL , ChenWY. The emerging and diverse roles of sirtuins in cancer: a clinical perspective. Onco Targets Ther.6, 1399–1416 (2013).
   PubMed Web of Science ®Google Scholar
• Roth M , ChenWY. Sorting out functions of sirtuins in cancer. Oncogene33(13), 1609–1620 (2014).
   PubMed Web of Science ®Google Scholar
• O’callaghan C , VassilopoulosA. Sirtuins at the crossroads of stemness, aging, and cancer. Aging Cell16(6), 1208–1218 (2017).
   PubMed Web of Science ®Google Scholar
• Dali-Youcef N , LagougeM , FroelichS , KoehlC , SchoonjansK , AuwerxJ. Sirtuins: the ‘magnificent seven’, function, metabolism and longevity. Ann. Med.39(5), 335–345 (2007).
   PubMed Web of Science ®Google Scholar
• Houtkooper RH , PirinenE , AuwerxJ. Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol.13(4), 225–238 (2012).
   PubMed Web of Science ®Google Scholar
• Mei Z , ZhangX , YiJ , HuangJ , HeJ , TaoY. Sirtuins in metabolism, DNA repair and cancer. J. Exp. Clin. Cancer Res.35(1), 182 (2016).
   PubMedGoogle Scholar
• Chalkiadaki A , GuarenteL. The multifaceted functions of sirtuins in cancer. Nat. Rev. Cancer15(10), 608–624 (2015).
   PubMed Web of Science ®Google Scholar
• Rifai K , IdrissouM , DauresM , BignonYJ , Penault-LlorcaF , Bernard-GallonD. SIRT1 in colorectal cancer: a friend or foe?OMICS22(4), 298–300 (2018).
   PubMed Web of Science ®Google Scholar
• Rifai K , IdrissouM , Penault-LlorcaF , BignonYJ , Bernard-GallonD. Breaking down the contradictory roles of histone deacetylase SIRT1 in human breast cancer. Cancers (Basel)10(11), E409 (2018).
   PubMed Web of Science ®Google Scholar
• Rifai K , JudesG , IdrissouMet al. Dual SIRT1 expression patterns strongly suggests its bivalent role in human breast cancer. Oncotarget8(67), 110922–110930 (2017).
   PubMedGoogle Scholar
• Rifai K , JudesG , IdrissouMet al. SIRT1-dependent epigenetic regulation of H3 and H4 histone acetylation in human breast cancer. Oncotarget9(55), 30661–30678 (2018).
   PubMedGoogle Scholar
• Song NY , SurhYJ. Janus-faced role of SIRT1 in tumorigenesis. Ann. NY Acad. Sci.1271, 10–19 (2012).
   PubMed Web of Science ®Google Scholar
• Stunkel W , CampbellRM. Sirtuin 1 (SIRT1): the misunderstood HDAC. J. Biomol. Screen.16(10), 1153–1169 (2011).
   PubMedGoogle Scholar
• Fang Y , NichollMB. Sirtuin 1 in malignant transformation: friend or foe?Cancer Lett.306(1), 10–14 (2011).
   PubMed Web of Science ®Google Scholar
• Tate CR , RhodesLV , SegarHCet al. Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat. Breast Cancer Res.14(3), R79 (2012).
   PubMed Web of Science ®Google Scholar
• Siegel D , HusseinM , BelaniCet al. Vorinostat in solid and hematologic malignancies. J. Hematol. Oncol.2, 31 (2009).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Shi YK , LiZH , HanXQet al. The histone deacetylase inhibitor suberoylanilide hydroxamic acid induces growth inhibition and enhances taxol-induced cell death in breast cancer. Cancer Chemother. Pharmacol.66(6), 1131–1140 (2010).
   PubMed Web of Science ®Google Scholar
• Yardley DA , Ismail-KhanRR , MelicharBet al. Randomized Phase II, double-blind, placebo-controlled study of exemestane with or without entinostat in postmenopausal women with locally recurrent or metastatic estrogen receptor-positive breast cancer progressing on treatment with a nonsteroidal aromatase inhibitor. J. Clin. Oncol.31(17), 2128–2135 (2013).
   PubMed Web of Science ®Google Scholar
• Trapani D , EspositoA , CriscitielloCet al. Entinostat for the treatment of breast cancer. Expert Opin. Investig. Drugs26(8), 965–971 (2017).
   PubMed Web of Science ®Google Scholar
• Yoshida M , KijimaM , AkitaM , BeppuT. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem.265(28), 17174–17179 (1990).
   PubMed Web of Science ®Google Scholar
• Yoshida M , NomuraS , BeppuT. Effects of trichostatins on differentiation of murine erythroleukemia cells. Cancer Res.47(14), 3688–3691 (1987).
   PubMed Web of Science ®Google Scholar
• Wood M , RymarchykS , ZhengS , CenY. Trichostatin A inhibits deacetylation of histone H3 and p53 by SIRT6. Arch. Biochem. Biophys.638, 8–17 (2018).
   PubMed Web of Science ®Google Scholar
• Zhou YD , LiJ , DuLet al. Biochemical and anti-triple negative metastatic breast tumor cell properties of psammaplins. Mar. Drugs16(11), 442 (2018).
   PubMed Web of Science ®Google Scholar
• Soldi R , CohenAL , ChengL , SunY , MoosPJ , BildAH. A genomic approach to predict synergistic combinations for breast cancer treatment. Pharmacogenomics J.13(1), 94–104 (2013).
   PubMed Web of Science ®Google Scholar
• Travaglini L , VianL , BilliM , GrignaniF , NerviC. Epigenetic reprogramming of breast cancer cells by valproic acid occurs regardless of estrogen receptor status. Int. J. Biochem. Cell Biol.41(1), 225–234 (2009).
   PubMed Web of Science ®Google Scholar
• Zhang L , WangG , WangLet al. VPA inhibits breast cancer cell migration by specifically targeting HDAC2 and down-regulating Survivin. Mol. Cell. Biochem.361(1–2), 39–45 (2012).
   PubMed Web of Science ®Google Scholar
• Grozinger CM , ChaoED , BlackwellHE , MoazedD , SchreiberSL. Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem.276(42), 38837–38843 (2001).
   PubMed Web of Science ®Google Scholar
• Wang J , KimTH , AhnMYet al. Sirtinol, a class III HDAC inhibitor, induces apoptotic and autophagic cell death in MCF-7 human breast cancer cells. Int. J. Oncol.41(3), 1101–1109 (2012).
   PubMed Web of Science ®Google Scholar
• Le Corre L , ChalabiN , DelortL , BignonYJ , Bernard-GallonDJ. Resveratrol and breast cancer chemoprevention: molecular mechanisms. Mol. Nutr. Food Res.49(5), 462–471 (2005).
   PubMed Web of Science ®Google Scholar
• Le Corre L , ChalabiN , DelortL , BignonYJ , Bernard-GallonDJ. Differential expression of genes induced by resveratrol in human breast cancer cell lines. Nutr. Cancer56(2), 193–203 (2006).
   PubMed Web of Science ®Google Scholar
• Fulda S , DebatinKM. Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene23(40), 6702–6711 (2004).
   PubMed Web of Science ®Google Scholar
• Chen KY , ChenCC , ChangYC , ChangMC. Resveratrol induced premature senescence and inhibited epithelial–mesenchymal transition of cancer cells via induction of tumor suppressor Rad9. PLoS ONE14(7), e0219317 (2019).
   PubMed Web of Science ®Google Scholar
• Chuang JC , JonesPA. Epigenetics and microRNAs. Pediatr. Res.61(5 Pt 2), 24R–29R (2007).
   PubMed Web of Science ®Google Scholar
• Iorio MV , FerracinM , LiuCGet al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res.65(16), 7065–7070 (2005).
   PubMed Web of Science ®Google Scholar
• De Rinaldis E , GazinskaP , MeraAet al. Integrated genomic analysis of triple-negative breast cancers reveals novel microRNAs associated with clinical and molecular phenotypes and sheds light on the pathways they control. BMC Genomics14, 643 (2013).
   PubMed Web of Science ®Google Scholar
• Finoux AL , ChartrandP. [Oncogenic and tumour suppressor microRNAs]. Med. Sci. (Paris)24(12), 1049–1054 (2008).
   PubMed Web of Science ®Google Scholar
• Hosseinahli N , AghapourM , DuijfPHG , BaradaranB. Treating cancer with microRNA replacement therapy: a literature review. J. Cell. Physiol.233(8), 5574–5588 (2018).
   PubMed Web of Science ®Google Scholar
• Swellam M , MahmoudMS , HashimM , HassanNM , SobeihME , NageebAM. Clinical aspects of circulating miRNA-335 in breast cancer patients: a prospective study. J. Cell. Biochem.120(6), 8975–8982 (2019).
   PubMed Web of Science ®Google Scholar
• Swellam M , ZahranRFK , AboEl-Sadat Taha H , El-KhazragyN , Abdel-MalakC. Role of some circulating MiRNAs on breast cancer diagnosis. Arch. Physiol. Biochem.125(5), 456–464 (2019).
   PubMed Web of Science ®Google Scholar
• Umeh-Garcia M , SimionC , HoPYet al. A novel bioengineered miR-127 prodrug suppresses the growth and metastatic potential of triple-negative breast cancer cells. Cancer Res.80(3), 418–429 (2020).
   PubMed Web of Science ®Google Scholar
• Gambari R , BrognaraE , SpandidosDA , FabbriE. Targeting oncomiRNAs and mimicking tumor suppressor miRNAs: new trends in the development of miRNA therapeutic strategies in oncology (Review). Int. J. Oncol.49(1), 5–32 (2016).
   PubMed Web of Science ®Google Scholar
• Swellam M , ElMagdoub HM , HassanNM , HefnyMM , SobeihME. Potential diagnostic role of circulating MiRNAs in breast cancer: implications on clinicopathological characters. Clin. Biochem.56, 47–54 (2018).
   PubMed Web of Science ®Google Scholar
• Ma L , ReinhardtF , PanEet al. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol.28(4), 341–347 (2010).
   PubMed Web of Science ®Google Scholar