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Although selective inhibitors of YTHDC1 have been reported, whether targeted degradation of YTHDC1 could achieve enhanced therapeutic efficacy remains unexplored. Here, we report the rational design and synthesis of the first PROTAC molecule targeting YTHDC1, termed XY-2, which was developed based on the cocrystal structure of YTHDC1 bound to its known inhibitor. XY-2 efficiently induced proteasome-dependent degradation of YTHDC1 at low nanomolar concentrations, with DC50 values of 11.42 nM in MOLM13 and 13.59 nM in Kasumi-1 cells. Functionally, XY-2 markedly inhibited proliferation, migration, and invasion, while robustly promoting apoptosis in multiple AML cell lines, with superior potency compared to its parent inhibitor. Transcriptomic and mechanistic analyses revealed that XY-2 downregulated genes associated with cell cycle, DNA replication, and mitotic progression, leading to G1 phase arrest. These findings establish XY-2 as the first highly efficient degrader of YTHDC1 and highlight targeted degradation of YTHDC1 as a promising therapeutic strategy for AML.<\/jats:p>","DOI":"10.1021\/jacsau.6c00278","type":"journal-article","created":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T16:39:44Z","timestamp":1781109584000},"page":"3778-3789","source":"Crossref","is-referenced-by-count":0,"title":["Development of the\nFirst YTHDC1 Degrader with Improved\nAntileukemia Activity"],"prefix":"10.1021","volume":"6","author":[{"given":"Zhongpao","family":"Xie","sequence":"first","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanyuan","family":"Zhang","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weicai","family":"Song","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qianqian","family":"Qi","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Xiong","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingyu","family":"Liu","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0605-8495","authenticated-orcid":true,"given":"Xiaocheng","family":"Weng","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1829-9368","authenticated-orcid":true,"given":"Xiang","family":"Zhou","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0340-230X","authenticated-orcid":true,"given":"Tian","family":"Tian","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430072"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,6,10]]},"reference":[{"key":"2026073100175732200_cit1","doi-asserted-by":"publisher","first-page":"332","DOI":"10.3390\/cancers14020332","article-title":"The Role of N6-Methyladenosine (m6A) Methylation\nModifications in Hematological Malignancies","volume":"14","author":"Zhao","year":"2022","journal-title":"Cancers"},{"key":"2026073100175732200_cit2","doi-asserted-by":"publisher","first-page":"764","DOI":"10.1016\/j.cell.2022.02.007","article-title":"The epitranscriptome toolbox","volume":"185","author":"Moshitch-Moshkovitz","year":"2022","journal-title":"Cell"},{"key":"2026073100175732200_cit3","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1038\/s41583-019-0244-z","article-title":"The m6A epitranscriptome: transcriptome plasticity in brain development\nand function","volume":"21","author":"Livneh","year":"2020","journal-title":"Nat. Rev. Neurosci."},{"key":"2026073100175732200_cit4","doi-asserted-by":"publisher","first-page":"1187","DOI":"10.1016\/j.cell.2017.05.045","article-title":"Dynamic RNA Modifications\nin Gene Expression Regulation","volume":"169","author":"Roundtree","year":"2017","journal-title":"Cell"},{"key":"2026073100175732200_cit5","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2021.629560","article-title":"YTH Domain Proteins:\nA Family of m6A Readers in Cancer Progression","volume":"11","author":"Xu","year":"2021","journal-title":"Frontiers in Oncology"},{"key":"2026073100175732200_cit6","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1186\/s12943-020-01233-2","article-title":"Novel insights\ninto\nthe interplay between m6A modification and noncoding RNAs\nin cancer","volume":"19","author":"Yi","year":"2020","journal-title":"Mol. Cancer"},{"key":"2026073100175732200_cit7","doi-asserted-by":"publisher","first-page":"3909","DOI":"10.1091\/mbc.10.11.3909","article-title":"The Interaction and\nColocalization\nof Sam68 with the Splicing-associated Factor YT521-B in Nuclear Dots\nIs Regulated by the Src Family Kinase p59fyn","volume":"10","author":"Hartmann","year":"1999","journal-title":"Mol. Biol. Cell"},{"key":"2026073100175732200_cit8","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1038\/nature18298","article-title":"Structural basis of N6-adenosine methylation\nby the METTL3-METTL14 complex","volume":"534","author":"Wang","year":"2016","journal-title":"Nature"},{"key":"2026073100175732200_cit9","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.31311","article-title":"YTHDC1 mediates nuclear export of\nN6-methyladenosine methylated mRNAs","volume":"6","author":"Roundtree","year":"2017","journal-title":"eLife"},{"key":"2026073100175732200_cit10","doi-asserted-by":"publisher","first-page":"1318","DOI":"10.1080\/15548627.2021.1974175","article-title":"m6A reader\nYTHDC1 modulates\nautophagy by targeting SQSTM1 in diabetic skin","volume":"18","author":"Liang","year":"2022","journal-title":"Autophagy"},{"key":"2026073100175732200_cit11","doi-asserted-by":"publisher","first-page":"2838","DOI":"10.1182\/blood.2021011707","article-title":"A critical\nrole of nuclear m6A reader YTHDC1 in leukemogenesis by\nregulating MCM complex-mediated DNA replication","volume":"138","author":"Sheng","year":"2021","journal-title":"Blood"},{"key":"2026073100175732200_cit12","doi-asserted-by":"publisher","first-page":"1014","DOI":"10.1158\/0008-5472.CAN-20-1876","article-title":"Therapeutic Targeting\nof Metadherin Suppresses Colorectal and Lung Cancer Progression and\nMetastasis","volume":"81","author":"Shen","year":"2021","journal-title":"Cancer Res."},{"key":"2026073100175732200_cit13","doi-asserted-by":"publisher","first-page":"3105","DOI":"10.1038\/s41418-021-00804-0","article-title":"YTHDC1-mediated augmentation\nof miR-30d in repressing pancreatic\ntumorigenesis via attenuation of RUNX1-induced transcriptional activation\nof Warburg effect","volume":"28","author":"Hou","year":"2021","journal-title":"Cell Death & Differentiation"},{"key":"2026073100175732200_cit14","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1038\/s41419-020-02795-1","article-title":"Nuclear export of\nchimeric mRNAs depends on an lncRNA-triggered autoregulatory loop\nin blood malignancies","volume":"11","author":"Chen","year":"2020","journal-title":"Cell Death Dis."},{"key":"2026073100175732200_cit15","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1038\/s41419-020-03186-2","article-title":"YTHDC1 mitigates ischemic\nstroke by promoting Akt phosphorylation\nthrough destabilizing PTEN mRNA","volume":"11","author":"Zhang","year":"2020","journal-title":"Cell Death\nDis."},{"key":"2026073100175732200_cit16","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2021.774305","article-title":"Low Expression\nof YTH Domain-Containing 1 Promotes Microglial M1 Polarization by\nReducing the Stability of Sirtuin 1 mRNA","volume":"15","author":"Zhou","year":"2021","journal-title":"Frontiers\nin Cellular Neuroscience"},{"key":"2026073100175732200_cit17","doi-asserted-by":"publisher","first-page":"100412","DOI":"10.1016\/j.jbo.2022.100412","article-title":"MiR-451a promotes cell growth, migration\nand EMT in\nosteosarcoma by regulating YTHDC1-mediated m6A methylation\nto activate the AKT\/mTOR signaling pathway","volume":"33","author":"Cao","year":"2022","journal-title":"Journal of Bone Oncology"},{"key":"2026073100175732200_cit18","doi-asserted-by":"publisher","first-page":"10879","DOI":"10.1111\/jcmm.16955","article-title":"Depletion\nof m6A reader protein YTHDC1 induces dilated cardiomyopathy\nby abnormal splicing of Titin","volume":"25","author":"Gao","year":"2021","journal-title":"Journal of Cellular\nand Molecular Medicine"},{"key":"2026073100175732200_cit19","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.00097-21","article-title":"The RNA Binding\nProteins YTHDC1 and FMRP Regulate the Nuclear Export of N6-Methyladenosine-Modified Hepatitis B Virus Transcripts and Affect\nthe Viral Life Cycle","volume":"95","author":"Kim","year":"2021","journal-title":"J. Virol."},{"key":"2026073100175732200_cit20","doi-asserted-by":"publisher","first-page":"578","DOI":"10.3892\/ol.2021.12839","article-title":"LINC00857 promotes cell proliferation and migration\nin colorectal cancer by interacting with YTHDC1 and stabilizing SLC7A5","volume":"22","author":"Tang","year":"2021","journal-title":"Oncol. Lett."},{"key":"2026073100175732200_cit21","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1038\/s41392-022-00905-3","article-title":"Nuclear Aurora kinase\nA switches\nm6A reader YTHDC1 to enhance an oncogenic RNA splicing\nof tumor suppressor RBM4","volume":"7","author":"Li","year":"2022","journal-title":"Signal Transduct.\nTarget. Ther."},{"key":"2026073100175732200_cit22","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1007\/s11262-022-01889-6","article-title":"Overexpression of m6A-factors METTL3, ALKBH5,\nand YTHDC1 alters HPV16 mRNA splicing","volume":"58","author":"Cui","year":"2022","journal-title":"Virus\nGenes"},{"key":"2026073100175732200_cit23","doi-asserted-by":"publisher","first-page":"958","DOI":"10.1016\/j.ccell.2021.04.017","article-title":"N6-Methyladenosine on mRNA facilitates a phase-separated nuclear body\nthat suppresses myeloid leukemic differentiation","volume":"39","author":"Cheng","year":"2021","journal-title":"Cancer Cell"},{"key":"2026073100175732200_cit24","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1038\/s41420-022-00947-0","article-title":"Insight into the structure, physiological function, and role in cancer\nof m6A readers-YTH domain-containing proteins","volume":"8","author":"Liao","year":"2022","journal-title":"Cell Death Discov."},{"key":"2026073100175732200_cit25","doi-asserted-by":"publisher","DOI":"10.3389\/fendo.2021.778875","article-title":"m6A Regulators in Human\nAdipose Tissue-Depot-Specificity and Correlation\nWith Obesity","volume":"12","author":"Ro\u0337nningen","year":"2021","journal-title":"Front. Endocrinol."},{"key":"2026073100175732200_cit26","doi-asserted-by":"publisher","DOI":"10.3389\/fphar.2022.933332","article-title":"The Role of m6A RNA Methylation in Cancer: Implication\nfor Nature Products Anti-Cancer\nResearch","volume":"13","author":"Song","year":"2022","journal-title":"Frontiers in Pharmacology"},{"key":"2026073100175732200_cit27","doi-asserted-by":"publisher","first-page":"746","DOI":"10.1016\/j.gendis.2020.07.011","article-title":"The critical\nroles of m6A modification in metabolic abnormality and\ncardiovascular diseases","volume":"8","author":"Zhang","year":"2021","journal-title":"Genes & Diseases"},{"key":"2026073100175732200_cit28","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1021\/acschembio.9b00894","article-title":"Selectively\nDisrupting m6A-Dependent Protein-RNA Interactions with\nFragments","volume":"15","author":"Bedi","year":"2020","journal-title":"ACS Chem. Biol."},{"key":"2026073100175732200_cit29","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejmcr.2022.100057","article-title":"Structure-based design\nof ligands of the m6A-RNA reader YTHDC1","volume":"5","author":"Li","year":"2022","journal-title":"European Journal of Medicinal Chemistry Reports"},{"key":"2026073100175732200_cit30","doi-asserted-by":"publisher","first-page":"9516","DOI":"10.1021\/acs.jmedchem.4c00599","article-title":"Structure-Based Design of a Potent\nand Selective YTHDC1 Ligand","volume":"67","author":"Za\u0301les\u030ca\u0301k","year":"2024","journal-title":"J. Med. Chem."},{"key":"2026073100175732200_cit31","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1042\/BJ20141450","article-title":"Targeting Cullin-RING\nE3 ubiquitin ligases for drug\ndiscovery: structure, assembly and small-molecule modulation","volume":"467","author":"Bulatov","year":"2015","journal-title":"Biochem. J."},{"key":"2026073100175732200_cit32","doi-asserted-by":"publisher","first-page":"8554","DOI":"10.1073\/pnas.141230798","article-title":"Protacs: Chimeric molecules that target proteins to\nthe Skp1-Cullin-F box complex for ubiquitination and degradation","volume":"98","author":"Sakamoto","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026073100175732200_cit33","doi-asserted-by":"publisher","first-page":"1966","DOI":"10.1002\/anie.201507978","article-title":"Small-Molecule PROTACS:\nNew Approaches to Protein Degradation","volume":"55","author":"Toure","year":"2016","journal-title":"Angew.\nChem., Int. Ed."},{"key":"2026073100175732200_cit34","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1002\/cbf.3369","article-title":"The PROTAC technology in drug development","volume":"37","author":"Zou","year":"2019","journal-title":"Cell Biochemistry and Function"},{"key":"2026073100175732200_cit35","doi-asserted-by":"publisher","DOI":"10.1016\/j.cclet.2024.109577","article-title":"Developing selective PI3K degraders to modulate both\nkinase and non-kinase functions","volume":"35","author":"Yang","year":"2024","journal-title":"Chin. Chem.\nLett."},{"key":"2026073100175732200_cit36","doi-asserted-by":"publisher","first-page":"6952","DOI":"10.1021\/acs.jmedchem.3c02195","article-title":"Discovery of Highly Potent and Efficient\nCBP\/p300 Degraders with Strong In Vivo Antitumor Activity","volume":"67","author":"Hu","year":"2024","journal-title":"J. Med. Chem."},{"key":"2026073100175732200_cit37","doi-asserted-by":"publisher","first-page":"8099","DOI":"10.1021\/acs.jmedchem.4c00193","article-title":"Design of FK866-Based Degraders for\nBlocking the Nonenzymatic Functions of Nicotinamide Phosphoribosyltransferase","volume":"67","author":"Lu","year":"2024","journal-title":"J. Med. Chem."},{"key":"2026073100175732200_cit38","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1126\/science.1233606","article-title":"Monitoring Drug Target\nEngagement in Cells and Tissues Using the Cellular Thermal Shift Assay","volume":"341","author":"Molina","year":"2013","journal-title":"Science"},{"key":"2026073100175732200_cit39","doi-asserted-by":"publisher","DOI":"10.1016\/j.gene.2024.148281","article-title":"The METTL3-m6A-YTHDC1-AMIGO2 axis contributes\nto cell proliferation and migration in esophageal squamous cell carcinoma","volume":"908","author":"Qiu","year":"2024","journal-title":"Gene"},{"key":"2026073100175732200_cit40","doi-asserted-by":"publisher","first-page":"16579","DOI":"10.1021\/acs.jmedchem.3c00104","article-title":"AcGlcAs: A Novel P53-Targeting\nArsenical with Potent Cellular Uptake and Cancer Cell Selectivity","volume":"66","author":"Liang","year":"2023","journal-title":"J. Med. Chem."},{"key":"2026073100175732200_cit41","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1038\/s41375-024-02451-z","article-title":"YTHDC1 is a therapeutic\ntarget for B-cell acute lymphoblastic leukemia by attenuating DNA\ndamage response through the KMT2C-H3K4me1\/me3 epigenetic axis","volume":"39","author":"Li","year":"2025","journal-title":"Leukemia"},{"key":"2026073100175732200_cit42","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1007\/s10565-024-09859-4","article-title":"YTHDC1 promotes the\nmalignant progression of gastric cancer by promoting\nROD1 translocation to the nucleus","volume":"40","author":"Dong","year":"2024","journal-title":"Cell Biol.\nToxicol."}],"container-title":["JACS Au"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/jacsau.6c00278","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jaaucr\/article-pdf\/6\/7\/3778\/66280736\/jacsau.6c00278.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jaaucr\/article-pdf\/6\/7\/3778\/66280736\/jacsau.6c00278.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T04:18:04Z","timestamp":1785471484000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jaaucr\/article\/6\/7\/3778\/5234010\/Development-of-the-First-YTHDC1-Degrader-with"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,10]]},"references-count":42,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2026,6,10]]},"published-print":{"date-parts":[[2026,7,27]]}},"URL":"https:\/\/doi.org\/10.1021\/jacsau.6c00278","relation":{},"ISSN":["2691-3704"],"issn-type":[{"value":"2691-3704","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,10]]}}}