Alteration of DNA Methyltransferases by Eribulin Elicits Broad DNA Methylation Changes with Potential Therapeutic Implications for Triple-Negative Breast Cancer

References

• Nguyen HT , Huynh LAK , Nguyen TV et al. Multimodal analysis of ctDNA methylation and fragmentomic profiles enhances detection of nonmetastatic colorectal cancer. Future Oncol. 18(35), 3895–3912 (2022).
   PubMed Web of Science ®Google Scholar
• Lehmann BD , Bauer JA , Chen X et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121(7), 2750–67 (2011).
   PubMed Web of Science ®Google Scholar
• Foulkes WD , Smith IE , Reis-Filho JS . Triple-negative breast cancer. N. Engl. J. Med. 363(20), 1938–48 (2010).
   PubMed Web of Science ®Google Scholar
• Houvenaeghel G , Sabatier R , Reyal F , Classe JM et al. Axillary lymph node micrometastases decrease triple-negative early breast cancer survival. Br. J. Cancer 115(9), 1024–1031 (2016).
   PubMed Web of Science ®Google Scholar
• Wang N , Ma T , Yu B . Targeting epigenetic regulators to overcome drug resistance in cancers. Sig. Transduct. Target Ther. 8, 69 (2023).
   PubMed Web of Science ®Google Scholar
• Sharma S , Kelly TK , Jones PA . Epigenetics in cancer. Carcinogenesis 31(1), 27–36 (2010).
   PubMed Web of Science ®Google Scholar
• Sharma P , Kumar S . Metabolic reprogramming in triple-negative breast cancer. Front. Oncol. 10, 428 (2021).
   Google Scholar
• Branham MT , Marzese DM , Laurito SR et al. Methylation profile of triple-negative breast carcinomas. Oncogenesis 1(7), e17 (2012).
   PubMedGoogle Scholar
• Esteller M , Silva JM , Dominguez G et al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl Cancer Inst. 92(7), 564–9 (2000).
   PubMedGoogle Scholar
• Jones PA , Baylin SB . The epigenomics of cancer. Cell 128(4), 683–92 (2007).
   PubMed Web of Science ®Google Scholar
• Lu Y , Roy S , Nuovo G et al. Anti-microRNA-222 (anti-miR-222) and -181B suppress the growth of tamoxifen-resistant xenografts in mouse by targeting TIMP3 protein and modulating mitogenic signal. J. Biol. Chem. 293(10), 3588 (2011).
   Google Scholar
• Fackler MJ , Umbricht CB , Williams D et al. Genome-wide methylation analysis identifies genes specific to breast cancer hormone receptor status and risk of recurrence. Cancer Res. 71(19), 6195–207 (2011).
   PubMed Web of Science ®Google Scholar
• Ma Y , Chai N , Jiang Q et al. DNA methyltransferase mediates the hypermethylation of the microRNA 34a promoter and enhances the resistance of patient-derived pancreatic cancer cells to molecular targeting agents. Pharmacol. Res. 160, 105071 (2020).
   PubMed Web of Science ®Google Scholar
• Zhang Z , Wang G , Li Y et al. Recent progress in DNA methyltransferase inhibitors as anticancer agents. Front. Pharmacol. 13, 1072651 (2022).
   PubMed Web of Science ®Google Scholar
• Stewart ML , Tamayo P , Wilson AJ et al. KRAS genomic status predicts the sensitivity of ovarian cancer cells to decitabine. Cancer Res. 75(14), 2897–906 (2015).
   PubMed Web of Science ®Google Scholar
• US Food and Drug Administration . FDA approves eribulin mesylate injection for the treatment of breast cancer (2010). www.fda.gov/news-events/press-announcements/fda-approves-eribulin-mesylate-injection-treatment-breast-cancer
   Google Scholar
• Twelves C , Cortes J , Vahdat L et al. Efficacy of eribulin in women with metastatic breast cancer: a pooled analysis of two phase 3 studies. Breast Cancer Res. Treat. 149(1), 313 (2014).
   Web of Science ®Google Scholar
• Bagheri M , Mohamed GA , Pattabiraman DR et al. Pharmacological induction of mesenchymal–epithelial transition chemosensitizes breast cancer cells and prevents metastatic progression. bioRxiv doi: 10.1101/2023.04.19.537586 (2023) ( Preprint).
   Google Scholar
• Thiery JP , Acloque H , Huang RY , Nieto MA . Epithelial–mesenchymal transitions in development and disease. Cell 139(5), 871–90 (2009).
   PubMed Web of Science ®Google Scholar
• Nieto MA , Huang RY , Jackson RA , Thiery JP . EMT: 2016. Cell 166(1), 21–45 (2016).
   PubMed Web of Science ®Google Scholar
• Lee M , Brown SM , Wilkins MO , Pattabiraman RD , Christensen CB . Distinct cytosine modification profiles define epithelial-to-mesenchymal cell-state transitions. Epigenomics 14(9), 519–535 (2022).
   PubMed Web of Science ®Google Scholar
• Pascual T , Oliveira M , Villagrasa P et al. Neoadjuvant eribulin in HER2-negative early-stage breast cancer (SOLTI-1007-NeoEribulin): a multicenter, two-cohort, non-randomized phase II trial. NPJ Breast Cancer 7, 145 (2021).
   PubMed Web of Science ®Google Scholar
• Illumina Human methylation EPIC annotation to use with IlluminaHumanMethylationEPICB5manifest and minfi. https://github.com/achilleasNP/IlluminaHumanMethylationEPICanno.ilm10b5.hg38
   Google Scholar
• Zhou W , Triche JT , Laird WP , Shen H . SeSAMe: reducing artifactual detection of DNA methylation by Infinium BeadChips in genomic deletions. Nucleic Acids Res. 46(20), e123 (2018).
   PubMed Web of Science ®Google Scholar
• Xu Z , Niu L , Taylor JA . The ENmix DNA methylation analysis pipeline for Illumina BeadChip and comparisons with seven other preprocessing pipelines. Clin. Epigenet. 13(1), 216 (2021).
   PubMed Web of Science ®Google Scholar
• O’Sullivan DE , Johnson KC , Skinner L , Koestler DC , Christensen BC . Epigenetic and genetic burden measures are associated with tumor characteristics in invasive breast carcinoma. Epigenetics 11(5), 344–53 (2016).
   PubMed Web of Science ®Google Scholar
• Ritchie EM , Phipson B , Wu D et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43(7), e47 (2015).
   PubMed Web of Science ®Google Scholar
• McLean CY , Bristor D , Hiller M . GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495–501 (2010).
   PubMed Web of Science ®Google Scholar
• Yu G , Wang LG , Han Y , He QY . ClusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16, 284–287 (2012).
   PubMed Web of Science ®Google Scholar
• Wu T , Hu E , Xu S et al. ClusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2(3), 100141 (2021).
   Google Scholar
• Castro-Mondragon AJ , Riudavets-Puig R , Rauluseviciute L et al. JASPAR: the 9th release of the open-access transcription factor binding profiles database. Nucleic Acids Res. 50(D1), D165–D173 (2022).
   PubMed Web of Science ®Google Scholar
• Tan G , Lenhard B . TFBSTools: an R/bioconductor package for transcription factor binding site analysis. Bioinformatics 15, 1555–1556 (2016).
   Google Scholar
• Yang X , Lay F , Han H , Jones PA . Targeting DNA methylation for epigenetic therapy. Trends Pharmacol. Sci. 31, 536–546 (2010).
   PubMed Web of Science ®Google Scholar
• Rea M , Eckstein M , Eleazer R et al. Genome-wide DNA methylation reprogramming in response to inorganic arsenic links inhibition of CTCF binding, DNMT expression and cellular transformation. Sci Rep 7, 41474 (2017).
   PubMed Web of Science ®Google Scholar
• Cowling VH , Cole MD . E-cadherin repression contributes to c-Myc-induced epithelial cell transformation. Oncogene 26 (24), 3582–3586 (2007).
   PubMed Web of Science ®Google Scholar
• Hamadneh L , Abu-Irmaileh B , Al-Majawleh M , Bustanji Y , Jarrar Y , Al-Qirim T . Doxorubicin–paclitaxel sequential treatment: insights of DNA methylation and gene expression changes of luminal A and triple negative breast cancer cell lines. Mol. Cell. Biochem. 476, 3647–3654 (2021).
   PubMed Web of Science ®Google Scholar
• Pedersen CA , Cao MD , Fleischer T et al. DNA methylation changes in response to neoadjuvant chemotherapy are associated with breast cancer survival. Breast Cancer Res. 24, 43 (2022).
   PubMed Web of Science ®Google Scholar
• Yu J , Zayas J , Qin B , Wang L . Targeting DNA methylation for treating triple-negative breast cancer. Pharmacogenomics 20, 1151–1157 (2019).
   PubMed Web of Science ®Google Scholar
• Serrano-Gomez SJ , Maziveyi M , Alahari SK . Regulation of epithelial–mesenchymal transition through epigenetic and post-translational modifications. Mol. Cancer 15, 18 (2016).
   PubMed Web of Science ®Google Scholar
• Bianchini G , Balko JM , Mayer IA , Sanders ME , Gianni L . Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat. Rev. Clin. Oncol. 13, 674–690 (2016).
   PubMed Web of Science ®Google Scholar
• Bulle A , Dekervel J , Libbrecht L et al. Gemcitabine induces epithelial-to-mesenchymal transition in patient-derived pancreatic ductal adenocarcinoma xenografts. Am. J. Transl. Res. 15, 765–779 (2019).
   Google Scholar
• Chen T , Ueda Y , Dodge JE , Wang Z , Li E . Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23(16), 5594–5605 (2003).
   PubMed Web of Science ®Google Scholar
• Man X , Li Q , Wang B , Zhang H , Zhang S , Li Z . DNMT3A and DNMT3B in breast tumorigenesis and potential therapy. Front. Cell. Dev. Biol. 10, 916725 (2022).
   PubMed Web of Science ®Google Scholar
• Baylin S , Jones P . A decade of exploring the cancer epigenome– biological and translational implications. Nat. Rev. Cancer 11(10), 726–34 (2011).
   PubMed Web of Science ®Google Scholar
• Gu T , Lin X , Cullen SM et al. DNMT3A and TET1 cooperate to regulate promoter epigenetic landscapes in mouse embryonic stem cells. Genome Biol. 19(1), 88 (2018).
   PubMedGoogle Scholar
• Zolota V , Tzelepi V , Piperigkou Z et al. Epigenetic alterations in triple-negative breast cancer – the critical role of extracellular matrix. Cancers 13(4), 713 (2021).
   PubMed Web of Science ®Google Scholar
• Cheng Y , He C , Wang M et al. Targeting epigenetic regulators for cancer therapy: mechanisms and advances in clinical trials. Signal Transduct. Target. Ther. 4, 62 (2019).
   PubMed Web of Science ®Google Scholar
• Baylin SB , Jones PA . Epigenetic determinants of cancer. Cold. Spring. Harb. Perspect. Biol. 8(9), a019505 (2016).
   PubMed Web of Science ®Google Scholar
• Fang F , Turcan S , Rimner A , Kaufman A , Giri D , Morris LGT . Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci. Transl. Med. 3(75), 75ra25 (2011).
   PubMed Web of Science ®Google Scholar
• Foulks JM , Parnell KM , Nix RN et al. Epigenetic drug discovery: targeting DNA methyltransferases. J. Biomol. Screen. 17(1), 2–17 (2012).
   PubMedGoogle Scholar
• Krushkal J , Silvers T , Reinhold WC et al. Epigenome-wide DNA methylation analysis of small cell lung cancer cell lines suggests potential chemotherapy targets. Clin. Epigenet. 12, 93 (2020).
   PubMed Web of Science ®Google Scholar