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Review

Potential Epigenetic Modifications Implicated in Triple- To Quadruple-Negative Breast Cancer Transition: A Review

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Pages 711-726 | Received 22 Jan 2022, Accepted 04 Apr 2022, Published online: 27 Apr 2022

References

  • Kang SP , MartelM , HarrisLN. Triple negative breast cancer: current understanding of biology and treatment options. Curr. Opin. Obstet. Gynecol.20(1), 40–46 (2008).
  • Prat A , PinedaE , AdamoBet al. Clinical implications of the intrinsic molecular subtypes of breast cancer. The Breast24(Suppl. 2), S26–S35 (2015).
  • Khaled N , BidetY. New insights into the implication of epigenetic alterations in the EMT of triple negative breast cancer. Cancers11(4), 559 (2019).
  • Shimelis H , LaDucaH , HuCet al. Triple-negative breast cancer risk genes identified by multigene hereditary cancer panel testing. JNCI J. Natl Cancer Inst.110(8), 855–862 (2018).
  • Philipovskiy A , DwivediAK , GamezRet al. Association between tumor mutation profile and clinical outcomes among Hispanic Latina women with triple-negative breast cancer. PloS One15(9), e0238262 (2020).
  • Uscanga-Perales GI , Santuario-FacioSK , Sanchez-DominguezCNet al. Genetic alterations of triple negative breast cancer (TNBC) in women from northeastern Mexico. Oncol. Lett.17(3), 3581–3588 (2019).
  • Angajala A , MothershedE , DavisMBet al. Quadruple negative breast cancers (QNBC) demonstrate subtype consistency among primary and recurrent or metastatic breast cancer. Transl. Oncol.12(3), 493–501 (2019).
  • Wright N , AkinyemijuT , SubhedarPet al. Targeting risk factors for reducing the racially disparate burden in breast cancer. Front Biosci.11, 136–160 (2019).
  • Davis M , TripathiS , HughleyRet al. AR negative triple negative or ‘quadruple negative’ breast cancers in African American women have an enriched basal and immune signature. PloS One13(6), e0196909 (2018).
  • Huang M , WuJ , LingRet al. Quadruple negative breast cancer. Breast Cancer.27(4), 527–533 (2020).
  • Nandy D , RajamSM , DuttaD. A three layered histone epigenetics in breast cancer metastasis. Cell Biosci.10(1), 1–23 (2020).
  • Perreault AA , SprungerDM , VentersBJ. Epigenetic and transcriptional profiling of triple negative breast cancer. Sci. Data6(1), 1–9 (2019).
  • Al-Khanbashi M , Al-MoundhriM. Micro-ribonucleic acid and carcinogenesis: breast cancer as an example. Oncol. Rev.9(1), 279 (2015).
  • Shi Y , YangF , SunZet al. Differential microRNA expression is associated with androgen receptor expression in breast cancer. Mol. Med. Rep.15(1), 29–36 (2017).
  • Wu X , DingM , LinJ. Three-microRNA expression signature predicts survival in triple-negative breast cancer. Oncol. Lett.19(1), 301–308 (2020).
  • Bayraktar R , PichlerM , KanlikilicerPet al. “MicroRNA 603 acts as a tumor suppressor and inhibits triple-negative breast cancer tumorigenesis by targeting elongation factor 2 kinase. Oncotarget8(7), 11641 (2017).
  • Mo W , LiuQ , LinCCet al. mTOR inhibitors suppress homologous recombination repair and synergize with PARP inhibitors via regulating SUV39H1 in BRCA-proficient triple-negative breast cancer. Clin. Cancer Res.22(7), 1699–1712 (2016).
  • Silver DP , RichardsonAL , EklundACet al. Efficacy of neoadjuvant cisplatin in triple-negative breast cancer AC. J. Clin. Oncol.28(7), 1145 (2010).
  • Kaleem M , PerwaizM , NurSMet al. Epigenetics of triple-negative breast cancer via natural compounds. Curr. Med. Chem.29(8), 1436–1458 (2022).
  • Selmin OI , DonovanMG , StillwaterBJet al. Epigenetic regulation and dietary control of triple negative breast cancer. Front. Nutr.7, 159 (2020).
  • Emens LA , CruzC , EderJPet al. Long-term clinical outcomes and biomarker analyses of atezolizumab therapy for patients with metastatic triple-negative breast cancer: a phase 1 study. JAMA Oncol.5(1), 74–82 (2019).
  • Jiao X , WangM , ZhangZet al. Leronlimab, a humanized monoclonal antibody to CCR5, blocks breast cancer cellular metastasis and enhances cell death induced by DNA damaging chemotherapy. Breast Cancer Res.23(1), 1–15 (2021).
  • Saini G , BhattaraiS , GogineniKet al. Quadruple-negative breast cancer: an uneven playing field. JCO Glob. Oncol.6, 233–237 (2020).
  • Bhattarai S , SainiG , GogineniKet al. Quadruple-negative breast cancer: novel implications for a new disease. Breast Cancer Res.22(1), 1–11 (2020).
  • Jansson S , BendahlPO , GrabauDAet al. The three receptor tyrosine kinases c-KIT, VEGFR2 and PDGFRα, closely spaced at 4q12, show increased protein expression in triple-negative breast cancer. PLoS One9(7), e102176 (2014).
  • Johansson I , AaltonenKE , EbbessonAet al. Increased gene copy number of KIT and VEGFR2 at 4q12 in primary breast cancer is related to an aggressive phenotype and impaired prognosis. Genes Chromosomes Cancer51(4), 375–383 (2012).
  • Feng Y , SpeziaM , HuangSet al. “Breast cancer development and progression: risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis. Genes Dis.5(2), 77–106 (2018).
  • Hafez MM , Al-ShabanahOA , Al-RejaieSSet al. Increased hypermethylation of glutathione S-transferase P1, DNA-binding protein inhibitor, death associated protein kinase and paired box protein-5 genes in triple-negative breast cancer Saudi females. Asian Pac. J. Cancer Prev.16(2), 541–549 (2015).
  • Chen YC , SahooS , BrienRet al. Single-cell RNA-sequencing of migratory breast cancer cells: discovering genes associated with cancer metastasis. Analyst144(24), 7296–7309 (2019).
  • Moosavi A , ArdekaniAM. Role of epigenetics in biology and human diseases AM. Iran. Biomed. J.20(5), 246 (2016).
  • Yin L , DuanJJ , BianXW , YuS. Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Res.22(1), 1–13 (2020).
  • Kagara N , HuynhKT , KuoCet al. Epigenetic regulation of cancer stem cell genes in triple-negative breast cancer. Am. J. Pathol.181(1), 257–267 (2012).
  • Sharma S , KellyTK , JonesPA. Epigenetics in cancer. Carcinogenesis31(1), 27–36 (2010).
  • Ciriello G , SinhaR , HoadleyKAet al. The molecular diversity of luminal A breast tumors. Breast Cancer Res. Treat.141(3), 409–420 (2013).
  • Bareche Y , VenetD , IgnatiadisMet al. Unravelling triple-negative breast cancer molecular heterogeneity using an integrative multiomic analysis. Ann. Oncol.29(4), 895–902 (2018).
  • Dattilo MA , BenzoY , HerreraLMet al. Regulatory mechanisms leading to differential acyl-CoA synthetase 4 expression in breast cancer cells. Sci. Rep.9(1), 1–13 (2019).
  • Bao L , QianZ , LyngMBet al. Coexisting genomic aberrations associated with lymph node metastasis in breast cancer. J. Clin. Invest.128(6), 2310–2324 (2018).
  • Bhattarai S , SugitaBM , BortolettoSMet al. QNBC is associated with high genomic instability characterized by copy number alterations and miRNA deregulation. Int. J. Mol. Sci.22(21), 11548 (2021).
  • Sporikova Z , KoudelakovaV , TrojanecRet al. Genetic markers in triple-negative breast cancer. Clin. Breast Cancer18(5), e841–e850 (2018).
  • Shah SP , RothA , GoyaRet al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature486(7403), 395–399 (2012).
  • Koboldt D , FultonR , McLellanMet al. Comprehensive molecular portraits of human breast tumours. Nature490(7418), 61–70 (2012).
  • Couch FJ , HartSN , SharmaPet al. Inherited mutations in 17 breast cancer susceptibility genes among a large triple-negative breast cancer cohort unselected for family history of breast cancer. J. Clin. Oncol.33(4), 304 (2015).
  • Jones N , BonnetF , SfarSet al. Comprehensive analysis of PTEN status in breast carcinomas. Int. J. Cancer133(2), 323–334 (2013).
  • Fedele CG , OomsLM , HoMet al. Inositol polyphosphate 4-phosphatase II regulates PI3K/Akt signaling and is lost in human basal-like breast cancers. Proc. Natl Acad. Sci.107(51), 22231–22236 (2010).
  • McGhan LJ , McCulloughAE , ProtheroeCAet al. Androgen receptor-positive triple negative breast cancer: a unique breast cancer subtype. Ann. Surg. Oncol.21(2), 361–367 (2014).
  • Naderi A , Hughes-DaviesL. A functionally significant cross-talk between androgen receptor and ErbB2 pathways in estrogen receptor negative breast cancer. Neoplasia10(6), 542–548 (2008).
  • Sher G , SalmanNA , KhanAQ et al. Epigenetic andbreast cancer therapy: Promising diagnostic and therapeutic applications. Semin. Cancer Biol. (2020).
  • Kagara N , HuynhKT , KuoCet al. Epigenetic regulation of cancer stem cell genes in triple-negative breast cancer. Am. J. Pathol.181(1), 257–267 (2012).
  • Garrido-Castro AC , LinNU , PolyakK. Insights into molecular classifications of triple-negative breast cancer: improving patient selection for treatment. Cancer Discov.9(2), 176–198 (2019).
  • Kazim Z , WahabiK , PerwezAet al. PTEN genetic and epigenetic alterations define distinct subgroups in North Indian breast cancer patients. Asian Pac. J. Cancer Prev. APJCP20(1), 269 (2019).
  • Li G , WangD , MaWet al. Transcriptomic and epigenetic analysis of breast cancer stem cells. Epigenomics10(6), 765–783 (2018).
  • Zolota V , TzelepiV , PiperigkouZet al. Epigenetic alterations in triple-negative breast cancer – the critical role of extracellular matrix. Cancers13(4), 713 (2021).
  • Naldi I , TarantaM , GherardiniLet al. Novel epigenetic target therapy for prostate cancer: a preclinical study. PLoS One9(5), e98101 (2014).
  • Heard E , MartienssenRA. Transgenerational epigenetic inheritance: myths and mechanisms. Cell157(1), 95–109 (2014).
  • Dai X , MaR , ZhaoXet al. Epigenetic profiles capturing breast cancer stemness for triple negative breast cancer control. Epigenomics11(16), 1811–1825 (2019).
  • He J , PengR , YuanZet al. Prognostic value of androgen receptor expression in operable triple-negative breast cancer: a retrospective analysis based on a tissue microarray. Med. Oncol.29(2), 406–410 (2012).
  • Keyvani-Ghamsari S , KhorsandiK , RasulAet al. Current understanding of epigenetics mechanism as a novel target in reducing cancer stem cells resistance. Clin. Epigenetics13(1), 1–31 (2021).
  • Grønbaek K , HotherC , JonesPA. Epigenetic changes in cancer. APMIS Acta Pathol. Microbiol. Immunol. Scand.115(10), 1039–1059 (2007).
  • Temian DC , PopLA , IrimieAIet al. The epigenetics of triple-negative and basal-like breast cancer: current knowledge. J. Breast Cancer21(3), 233–243 (2018).
  • Llinàs-Arias P , Íñiguez-MuñozS , McCannKet al. Epigenetic regulation of immunotherapy response in triple-negative breast cancer. Cancers13(16), 4139 (2021).
  • Moghazy TF , ElattarHA , EldeebMKet al. Methylation of glutathione-S-transferase P1 promotor in Egyptian females with breast cancer. Asian Pac. J. Cancer Prev. APJCP20(8), 2523 (2019).
  • Morizono A , TanabeM , IkemuraMet al. Loss of BRCA1 expression and morphological features associated with BRCA1 promoter methylation status in triple-negative breast cancer. J. Hum. Genet.66(8), 785–793 (2021).
  • Prajzendanc K , DomagałaP , HybiakJet al. BRCA1 promoter methylation in peripheral blood is associated with the risk of triple-negative breast cancer. Int. J. Cancer146(5), 1293–1298 (2020).
  • Ruscito I , GasparriML , DeMarco MPet al. The clinical and pathological profile of BRCA1 gene methylated breast cancer women: a meta-analysis. Cancers13(6), 1391 (2021).
  • Al-Yousef N , ShinwariZ , Al-ShahraniBet al. Curcumin induces re-expression of BRCA1 and suppression of γ synuclein by modulating DNA promoter methylation in breast cancer cell lines. Oncol. Rep.43(3), 827–838 (2020).
  • Hon JDC , SinghB , SahinAet al. Breast cancer molecular subtypes: from TNBC to QNBC. Am. J. Cancer Res.6(9), 1864 (2016).
  • Velasco-Velázquez MA , HomsiN , DeLa Fuente M , PestellRG. Breast cancer stem cells. Int. J. Biochem. Cell Biol.44(4), 573–577 (2012).
  • Ralser DJ , KlümperN , GevenslebenHet al. Molecular and immune correlates of PDCD1 (PD-1), PD-L1 (CD274), and PD-L2 (PDCD1LG2) DNA methylation in triple negative breast cancer. J. Immunother.44(8), 319–324 (2021).
  • Wang F , CaoX , YinLet al. Identification of SCARA5 gene as a potential immune-related biomarker for triple-negative breast cancer by integrated analysis. DNA Cell Biol.39(10), 1813–1824 (2020).
  • Mittendorf EA , PhilipsAV , Meric-BernstamFet al. PD-L1 expression in triple-negative breast cance”. Cancer Immunol. Res.2(4), 361–370 (2014).
  • Kozomara Z , SupicG , KrivokucaAet al. Promoter hypermethylation of p16, BRCA1 and RASSF1A genes in triple-negative breast cancer patients from Serbia. J. BUON23, 684–691 (2018).
  • Manica GC , RibeiroCF , DeOliveira MAet al. Down regulation of ADAM33 as a predictive biomarker of aggressive breast cancer. Sci. Rep.7(1), 1–13 (2017).
  • Miyagawa Y , MatsushitaY , SuzukiHet al. Frequent downregulation of LRRC26 by epigenetic alterations is involved in the malignant progression of triple-negative breast cancer. Int. J. Oncol.52(5), 1539–1558 (2018).
  • Wang H , WuD , CaiLet al. Aberrant methylation of WD-repeat protein 41 contributes to tumour progression in triple-negative breast cancer. J. Cell. Mol. Med.24(12), 6869–6882 (2020).
  • Xia J , LüZD , ZhouPHet al. DNA methylation modification of BRMS1 in triple-negative breast cancer and its correlation with tumor metastasis. Zhonghua Yi Xue Za Zhi97(44), 3483–3487 (2017).
  • Paço A , Leitão-CastroJ , FreitasR. Epigenetic regulation of CDH1 is altered after HOXB7-silencing in MDA-MB-468 triple-negative breast cancer cells. Genes12(10), 1575 (2021).
  • Rozova VS , AnwerAG , GullerAEet al. Machine learning reveals mesenchymal breast carcinoma cell adaptation in response to matrix stiffness. PLoS Comput. Biol.17(7), e1009193 (2021).
  • Noyan S , OzketenAA , GurdalHet al. miR-770-5p regulates EMT and invasion in TNBC cells by targeting DNMT3A. Cell. Signal.83, 109996 (2021).
  • Roll JD , RivenbarkAG , JonesWDet al. DNMT3b overexpression contributes to a hypermethylator phenotype in human breast cancer cell lines. Mol. Cancer7(1), 1–14 (2008).
  • Cha Y , JungW , KooJ. Expression of DNA methylation-related proteins in metastatic breast cancer. Neoplasma64(3), 412–420 (2017).
  • 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).
  • Kim YJ , SungM , OhEet al. Engrailed 1 overexpression as a potential prognostic marker in quintuple-negative breast cancer. Cancer Biol. Ther.19(4), 335–345 (2018).
  • Schech A , KaziA , YuSet al. Histone deacetylase inhibitor entinostat inhibits tumor-initiating cells in triple-negative breast cancer cells. Mol. Cancer Ther.14(8), 1848–1857 (2015).
  • Yusuf AP , AbubakarMB , MalamiIet al. Zinc metalloproteins in epigenetics and their crosstalk. Life11(3), 186 (2021).
  • Zheng Q , FanH , MengZet al. Histone demethylase KDM2B promotes triple negative breast cancer proliferation by suppressing p15INK4B, p16INK4A, and p57KIP2 transcription. Acta Biochim. Biophys. Sin.50(9), 897–904 (2018).
  • Gao B , LiuX , LiZet al. Overexpression of EZH2/NSD2 histone methyltransferase axis predicts poor prognosis and accelerates tumor progression in triple-negative breast cancer. Front. Oncol.10, 3421 (2021).
  • Kundur S , PrayagA , SelvakumarPet al. Synergistic anticancer action of quercetin and curcumin against triple-negative breast cancer cell lines. J. Cell. Physiol.234(7), 11103–11118 (2019)
  • Bao C , LiuT , QianLet al. Shikonin inhibits migration and invasion of triple-negative breast cancer cells by suppressing epithelial–mesenchymal transition via miR-17-5p/PTEN/Akt pathway. J. Cancer12(1), 76 (2021).
  • Maiti A , QiQ , PengXet al. Class I histone deacetylase inhibitor suppresses vasculogenic mimicry by enhancing the expression of tumor suppressor and anti-angiogenesis genes in aggressive human TNBC cells. Int. J. Oncol.55(1), 116–130 (2019).
  • Loh HY , NormanBP , LaiKSet al. The regulatory role of microRNAs in breast cancer. Int. J. Mol. Sci.20(19), 4940 (2019).
  • Peng Y , CroceCM. The role of microRNAs in human cancer. Signal Transduct. Target. Ther.1, 15004 (2016).
  • Paul U , BanerjeeS. The functional significance and cross-talk of non-coding RNAs in triple negative and quadruple negative breast cancer. Mol. Biol. Rep.1–20 (2022).
  • Qattan A , Al-TweigeriT , SulemanK. Translational implications of dysregulated pathways and microRNA regulation in quadruple-negative breast cancer. Biomedicines10(2), 366 (2022).
  • Yao M , WangS , ChenLet al. Research on correlations of miR-585 expression with progression and prognosis of triple-negative breast cancer. Clin. Exp. Med.1–7 (2021).
  • Turashvili G , LightbodyED , TyryshkinKet al. Novel prognostic and predictive microRNA targets for triple-negative breast cancer. FASEB J.32(11), 5937–5954 (2018).
  • Wu J , ZhouZ. MicroRNA-432 acts as a prognostic biomarker and an inhibitor of cell proliferation, migration, and invasion in breast cancer. Clin. Breast Cancer.21(4), e462–e470 (2021).
  • Wang W , ZhangW , WuJet al. miR-522 regulates cell proliferation, migration, invasion capacities and acts as a potential biomarker to predict prognosis in triple-negative breast cancer. Clin. Exp. Med.1–8 (2021).
  • Gao S , ShiP , TianZet al. Overexpression of miR-1225 promotes the progression of breast cancer, resulting in poor prognosis. Clin. Exp. Med.21(2), 287–296 (2021).
  • Li HY , LiangJL , KuoYLet al. miR-105/93-3p promotes chemoresistance and circulating miR-105/93-3p acts as a diagnostic biomarker for triple negative breast cancer. Breast Cancer Res.19(1), 1–14 (2017).
  • Kleivi Sahlberg K , BottaiG , NaumeBet al. A serum microRNA signature predicts tumor relapse and survival in triple-negative breast cancer patients. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res.21(5), 1207–1214 (2015).
  • Lü L , MaoX , ShiPet al. MicroRNAs in the prognosis of triple-negative breast cancer: a systematic review and meta-analysis. Medicine (Baltimore)96(22), e7085 (2017).
  • Thakur S , GroverRK , GuptaSet al. Identification of specific miRNA signature in paired sera and tissue samples of Indian women with triple negative breast cancer. PloS One11(7), e0158946 (2016).
  • An P , LiJ , LuLet al. Histone deacetylase 8 triggers the migration of triple negative breast cancer cells via regulation of YAP signals. Eur. J. Pharmacol.845, 16–23 (2019).
  • Jarrard DF , KinoshitaH , ShiYet al. Methylation of the androgen receptor promoter CpG island is associated with loss of androgen receptor expression in prostate cancer cells. Cancer Res.58(23), 5310–5314 (1998).
  • Nakayama T , WatanabeM , SuzukiHet al. Epigenetic regulation of androgen receptor gene expression in human prostate cancers. Lab. Invest.80(12), 1789–1796 (2000).
  • Takahashi S , InagumaS , SakakibaraMet al. DNA methylation in the androgen receptor gene promoter region in rat prostate cancers. The Prostate52(1), 82–88 (2002).
  • Chu M , ChangY , LiPet al. Androgen receptor is negatively correlated with the methylation-mediated transcriptional repression of miR-375 in human prostate cancer cells. Oncol. Rep.31(1), 34–40 (2014).
  • Bandini E , FaniniF. MicroRNAs and androgen receptor: emerging players in breast cancer. Front. Genet.10, 203 (2019).
  • Nakano K , MikiY , HataSet al. Identification of androgen-responsive microRNAs and androgen-related genes in breast cancer. Anticancer Res.33(11), 4811–4819 (2013).
  • Yang F , ShenY , ZhangWet al. An androgen receptor negatively induced long non-coding RNA ARNILA binding to miR-204 promotes the invasion and metastasis of triple-negative breast cancer. Cell Death Differ.25(12), 2209–2220 (2018).
  • Kuwata H , NakataniE , Shimbara-MatsubayashiSet al. Long-chain acyl-CoA synthetase 4 participates in the formation of highly unsaturated fatty acid-containing phospholipids in murine macrophages. Biochim. Biophys. Acta BBA – Mol. Cell Biol. Lipids1864(11), 1606–1618 (2019).
  • Wu X , LiY , WangJet al. Long chain fatty acyl-CoA synthetase 4 is a biomarker for and mediator of hormone resistance in human breast cancer. PloS One8(10), e77060 (2013).
  • Monaco ME , CreightonCJ , LeePet al. Expression of long-chain fatty acyl-CoA synthetase 4 in breast and prostate cancers is associated with sex steroid hormone receptor negativity. Transl. Oncol.3(2), 91–98 (2010).
  • Talley JT , MohiuddinSS. Biochemistry, fatty acid oxidation. In: StatPearls [Internet]StatPearls Publishing, FL, USA (2021).
  • Garmpis N , DamaskosC , GarmpiAet al. Histone deacetylases as new therapeutic targets in triple-negative breast cancer: progress and promises. Cancer Genomics Proteomics14(5), 299–313 (2017).
  • Damaskos C , ValsamiS , SpartalisEet al. Histone deacetylase inhibitors: a novel therapeutic weapon against medullary thyroid cancer? Anticancer Res. 36(10), 5019–5024 (2016).
  • Wu S , LuoZ , YuPJet al. Suberoylanilide hydroxamic acid (SAHA) promotes the epithelial mesenchymal transition of triple negative breast cancer cells via HDAC8/FOXA1 signals. Biol. Chem.397(1), 75–83 (2016).
  • Kashiwagi S , YashiroM , TakashimaTet al. Significance of E-cadherin expression in triple-negative breast cancer. Br. J. Cancer103(2), 249–255 (2010).
  • Tang D , XuS , ZhangQet al. The expression and clinical significance of the androgen receptor and E-cadherin in triple-negative breast cancer. Med. Oncol.29(2), 526–533 (2012).
  • Tate CR , RhodesLV , SegarHCet al. Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat. Breast Cancer Res.14(3), 1–15 (2012).
  • Merino VF , NguyenN , JinKet al. Combined treatment with epigenetic, differentiating, and chemotherapeutic agents cooperatively targets tumor-initiating cells in triple-negative breast cancer. Cancer Res.76(7), 2013–2024 (2016).
  • Peluffo G , SubedeeA , HarperNWet al. EN1 is a transcriptional dependency in triple-negative breast cancer associated with brain metastasis. Cancer Res.79(16), 4173–4183 (2019).
  • Davie JR . Inhibition of histone deacetylase activity by butyrate. J. Nutr.133(Suppl. 7), S2485–S2493 (2003).
  • ElMoneim HMA , ZaghloulNM. Expression of E-cadherin, N-cadherin and snail and their correlation with clinicopathological variants: an immunohistochemical study of 132 invasive ductal breast carcinomas in Egypt. Clin. Sao Paulo Braz.66(10), 1765–1771 (2011).

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