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In this study, we show that ALKBH1 is overexpressed in acute myeloid leukemia (AML) and essential for leukemia stem cell\/leukemia-initiating cell self-renewal and AML development\/maintenance but dispensable for normal hematopoiesis. ALKBH1 enhances mitochondrial assembly\/function and oxidative phosphorylation, crucial for AML survival\/proliferation and resistance to venetoclax, a potent BCL2 inhibitor and widely used first-line targeted therapy for AML in the clinic. Mechanistically, ALKBH1 catalyzes 5-formylcytosine at tRNA wobble positions, reprograming decoding and facilitating codon-biased translation, a mechanism we term \u201cepitranslatomic Midas touch,\u201d which in turn drives leukemogenesis and drug resistance by promoting the synthesis of key oncogenic proteins like WDR43. Targeting ALKBH1, particularly together with venetoclax, exhibited potent antileukemia efficacy in preclinical models with favorable safety profiles. Collectively, our findings elucidate ALKBH1\u2019s pivotal role in codon-biased translation and tumorigenesis and propose a novel therapeutic strategy for cancer treatment.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Significance:<\/jats:title>\n                    <jats:p>This study uncovers that ALKBH1-driven tRNA-decoding reprogramming and codon-biased translation, termed \u201cepitranslatomic Midas touch,\u201d is crucial for leukemogenesis, leukemia stem cell\/leukemia-initiating cell self-renewal, mitochondria structure\/function, and resistance to venetoclax. Targeting ALKBH1, especially in combination with venetoclax, offers a promising therapeutic strategy to combat drug resistance in AML and potentially other ALKBH1-overexpressing cancers.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1158\/2159-8290.cd-24-1043","type":"journal-article","created":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T11:43:03Z","timestamp":1754048583000},"page":"2298-2325","update-policy":"https:\/\/doi.org\/10.1158\/crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["ALKBH1 Drives Tumorigenesis and Drug Resistance via tRNA-decoding Reprogramming and Codon-biased Translation"],"prefix":"10.1158","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9406-7075","authenticated-orcid":false,"given":"Chao","family":"Shen","sequence":"first","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and Therapeutics, Beckman Research Institute of City of Hope, Monrovia, California."},{"name":"2Hangzhou Institute of Medicine, Chinese Academy of Sciences, Hangzhou, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9595-1567","authenticated-orcid":false,"given":"Yuan","family":"Che","sequence":"additional","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and Therapeutics, Beckman Research Institute of City of Hope, Monrovia, California."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7905-3399","authenticated-orcid":false,"given":"Keren","family":"Zhou","sequence":"additional","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and Therapeutics, Beckman Research Institute of City of Hope, Monrovia, California."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-0485-0853","authenticated-orcid":false,"given":"Kitty","family":"Wang","sequence":"additional","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and Therapeutics, Beckman Research Institute of City of Hope, Monrovia, California."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0672-7473","authenticated-orcid":false,"given":"Wei","family":"Li","sequence":"additional","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and Therapeutics, Beckman Research Institute of City of Hope, Monrovia, California."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-5876-1486","authenticated-orcid":false,"given":"Diyuan","family":"Xue","sequence":"additional","affiliation":[{"name":"1Department of Systems Biology and Center for RNA Biology and 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