{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T13:08:58Z","timestamp":1785330538051,"version":"3.55.0"},"reference-count":50,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:00:00Z","timestamp":1785283200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:00:00Z","timestamp":1785283200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82473109"],"award-info":[{"award-number":["82473109"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["42361144793"],"award-info":[{"award-number":["42361144793"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021171","name":"Basic and Applied Basic Research Foundation of Guangdong Province","doi-asserted-by":"publisher","award":["2025A1515012357"],"award-info":[{"award-number":["2025A1515012357"]}],"id":[{"id":"10.13039\/501100021171","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021171","name":"Basic and Applied Basic Research Foundation of Guangdong Province","doi-asserted-by":"publisher","award":["2024A1515013266"],"award-info":[{"award-number":["2024A1515013266"]}],"id":[{"id":"10.13039\/501100021171","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100018554","name":"Science and Technology Program of Gansu Province","doi-asserted-by":"publisher","award":["23ZDFA003"],"award-info":[{"award-number":["23ZDFA003"]}],"id":[{"id":"10.13039\/501100018554","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["advanced.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Advanced Science"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Metabolic reprogramming toward enhanced aerobic glycolysis is a hallmark of cancer, yet the contribution of ubiquitin\u2010like modifications to this process remains poorly understood. Here, we identify the UFMylation E3 ligase UFL1 as a critical suppressor of glycolytic metabolism and colorectal cancer (CRC) progression. Mechanistically, UFL1 directly interacts with the glycolytic enzyme enolase 1 (ENO1) and catalyzes its UFMylation at lysine residues K285 and K420. This modification disrupts ENO1 dimerization, attenuates its enzymatic activity, and consequently suppresses glycolytic flux. Functionally, UFL1\u2010mediated UFMylation inhibits tumor growth both in vitro and in vivo. Notably, pharmacological enhancement of the UFL1\u2010ENO1 interaction using the FDA\u2010approved antibiotic torezolid significantly potentiates the antitumor efficacy of 5\u2010fluorouracil (5\u2010FU) across multiple preclinical models, including CRC patient\u2010derived organoids and xenografts, without detectable toxicity. Collectively, these findings identify ENO1 as a direct substrate of UFMylation, establish UFMylation as a previously unrecognized regulator of cancer metabolic reprogramming, and highlight the UFL1\u2010ENO1 axis as a promising therapeutic target for colorectal cancer.<\/jats:p>","DOI":"10.1002\/advs.76875","type":"journal-article","created":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T12:42:51Z","timestamp":1785328971000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["UFL1\u2010Mediated UFMylation of ENO1 Restrains Aerobic Glycolysis and Colorectal Cancer Progression"],"prefix":"10.1002","author":[{"given":"Xiuqing","family":"Ma","sequence":"first","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui","family":"Wan","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yueyuan","family":"Zhong","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziyang","family":"Cui","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Venereology Peking University First Hospital Peking University  Beijing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuan","family":"Zhang","sequence":"additional","affiliation":[{"name":"School of Pharmacy Lanzhou University  Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqiang","family":"He","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"},{"name":"Guangdong Engineering Research Center of Chinese Medicine and Disease Susceptibility College of Pharmacy Jinan University  Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Huang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wan\u2010Yang","family":"Sun","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"},{"name":"Guangdong Engineering Research Center of Chinese Medicine and Disease Susceptibility College of Pharmacy Jinan University  Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5505-5672","authenticated-orcid":false,"given":"Rong\u2010Rong","family":"He","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"},{"name":"Guangdong Engineering Research Center of Chinese Medicine and Disease Susceptibility College of Pharmacy Jinan University  Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4167-6413","authenticated-orcid":false,"given":"Yang","family":"Zhou","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianshuang","family":"Li","sequence":"additional","affiliation":[{"name":"College of Life Science and Technology Jinan University  Guangzhou Guangdong China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Shen","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Engineering Technology Research Center for Innovative Drugs and Bioproducts School of Pharmacy Guangdong Medical University Dongguan Guangdong China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4347-8245","authenticated-orcid":false,"given":"Shao\u2010Hua","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Pharmacy Lanzhou University  Lanzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tongzheng","family":"Liu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Bioactive Molecules and Druggability Assessment Guangdong Basic Research Center of Excellence for Natural Bioactive Molecules and Discovery of Innovative Drugs College of Pharmacy Jinan University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,7,29]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"publisher","DOI":"10.3322\/caac.21834"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2021.0106"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.canlet.2024.217156"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.drup.2018.03.001"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13045\u2010022\u201001358\u20105"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12967\u2010024\u201005847\u20108"},{"key":"e_1_2_10_8_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.phrs.2019.104511"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1172\/jci69741"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pharmthera.2024.108680"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M610590200"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2022.111168"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbc.2022.102016"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41422\u2010019\u20100236\u20106"},{"key":"e_1_2_10_15_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41556\u2010020\u20100559\u2010z"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010019\u201009175\u20100"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2024.01.024"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41588\u2010020\u20100636\u2010z"},{"key":"e_1_2_10_19_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010022\u201035501\u20100"},{"key":"e_1_2_10_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2025.116433"},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.apsb.2022.05.019"},{"key":"e_1_2_10_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.omto.2021.12.026"},{"key":"e_1_2_10_23_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M110.172171"},{"key":"e_1_2_10_24_1","doi-asserted-by":"publisher","DOI":"10.1038\/cdd.2015.51"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2020.02.017"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1136\/jitc\u20102022\u2010005668"},{"key":"e_1_2_10_27_1","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkz110"},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.semcancer.2021.03.010"},{"key":"e_1_2_10_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2025.11.030"},{"key":"e_1_2_10_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbc.2022.102654"},{"key":"e_1_2_10_31_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M112.349274"},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.7150\/ijbs.63556"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.1038\/s43018\u2010021\u201000299\u20101"},{"key":"e_1_2_10_34_1","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.3572"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13045\u2010016\u20100385\u20108"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/s0014\u20105793(00)01494\u20100"},{"key":"e_1_2_10_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2016.04.009"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/mco2.245"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2022.05.019"},{"key":"e_1_2_10_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2018.04.011"},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2408354121"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.7150\/ijbs.90774"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.apsb.2025.03.041"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1021\/cb300687k"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41419\u2010020\u201003087\u20104"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1158\/1535\u20107163.Mct\u201021\u20100285"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40265\u2010015\u20100352\u20107"},{"key":"e_1_2_10_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2019.05.031"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41592\u2010019\u20100619\u20100"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.4463"},{"key":"e_1_2_10_51_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41556\u2010023\u201001185\u2010x"}],"container-title":["Advanced Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/advs.76875","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/advs.76875","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/advs.76875","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T12:42:52Z","timestamp":1785328972000},"score":1,"resource":{"primary":{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/10.1002\/advs.76875"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,29]]},"references-count":50,"alternative-id":["10.1002\/advs.76875"],"URL":"https:\/\/doi.org\/10.1002\/advs.76875","archive":["Portico"],"relation":{},"ISSN":["2198-3844","2198-3844"],"issn-type":[{"value":"2198-3844","type":"print"},{"value":"2198-3844","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,29]]},"assertion":[{"value":"2026-04-06","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-07-08","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-07-29","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e76875"}}