{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,14]],"date-time":"2026-08-14T18:33:03Z","timestamp":1786732383408,"version":"build-2736575974"},"reference-count":58,"publisher":"American Chemical Society (ACS)","issue":"8","license":[{"start":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T00:00:00Z","timestamp":1657670400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T00:00:00Z","timestamp":1657670400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T00:00:00Z","timestamp":1657670400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/501100002973","name":"Daiichi-Sankyo","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002973","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["CA217809"],"award-info":[{"award-number":["CA217809"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000082","name":"Division of Graduate Education","doi-asserted-by":"publisher","award":["DGE-1656518"],"award-info":[{"award-number":["DGE-1656518"]}],"id":[{"id":"10.13039\/100000082","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,8,19]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Impaired DNA repair activity has been shown to greatly increase rates of cancer clinically. It has been hypothesized that upregulating repair activity in susceptible individuals may be a useful strategy for inhibiting tumorigenesis. Here, we report that selected tyrosine kinase (TK) inhibitors including nilotinib, employed clinically in the treatment of chronic myeloid leukemia, are activators of the repair enzyme Human MutT Homolog 1 (MTH1). MTH1 cleanses the oxidatively damaged cellular nucleotide pool by hydrolyzing the oxidized nucleotide 8-oxo-2\u2019-deoxyguanosine (8-oxo-dG)\u00adTP, which is a highly mutagenic lesion when incorporated into DNA. Structural optimization of analogues of TK inhibitors resulted in compounds such as SU0448, which induces 1000 \u00b1 100% activation of MTH1 at 10 \u03bcM and 410 \u00b1 60% at 5 \u03bcM. The compounds are found to increase the activity of the endogenous enzyme, and at least one (SU0448) decreases levels of 8-oxo-dG in cellular DNA. The results suggest the possibility of using MTH1 activators to decrease the frequency of mutagenic nucleotides entering DNA, which may be a promising strategy to suppress tumorigenesis in individuals with elevated cancer risks.<\/jats:p>","DOI":"10.1021\/acschembio.2c00038","type":"journal-article","created":{"date-parts":[[2022,7,13]],"date-time":"2022-07-13T15:55:28Z","timestamp":1657727728000},"page":"2074-2087","source":"Crossref","is-referenced-by-count":14,"title":["Enhancing Repair\nof Oxidative DNA Damage with Small-Molecule\nActivators of MTH1"],"prefix":"10.1021","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2875-1773","authenticated-orcid":true,"given":"Yujeong","family":"Lee","sequence":"first","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshiyuki","family":"Onishi","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"McPherson","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna M.","family":"Kietrys","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marian","family":"Hebenbrock","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong Woong","family":"Jun","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ishani","family":"Das","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shanthi","family":"Adimoolam","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Debin","family":"Ji","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael G.","family":"Mohsen","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James M.","family":"Ford","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7310-2935","authenticated-orcid":true,"given":"Eric T.","family":"Kool","sequence":"additional","affiliation":[{"name":"Stanford University , , , ,","place":["Stanford, California, United States, 94305"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2022,7,13]]},"reference":[{"key":"2026081413075252800_cit1","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1038\/nature05978","article-title":"Base-Excision Repair of Oxidative\nDNA Damage","volume":"447","author":"David","year":"2007","journal-title":"Nature"},{"key":"2026081413075252800_cit2","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1126\/science.1905840","article-title":"P53 Mutations in Human\nCancers","volume":"253","author":"Hollstein","year":"1991","journal-title":"Science"},{"key":"2026081413075252800_cit3","first-page":"5291","article-title":"P53 Mutations in Breast Cancer","volume":"52","author":"Coles","year":"1992","journal-title":"Cancer Res."},{"key":"2026081413075252800_cit4","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1016\/j.dnarep.2010.03.004","article-title":"Oxygen as a Friend and Enemy: How\nto Combat the Mutational Potential of 8-Oxo-Guanine","volume":"9","author":"van\nLoon","year":"2010","journal-title":"DNA Repair"},{"key":"2026081413075252800_cit5","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1111\/j.1349-7006.2007.00409.x","article-title":"Significance\nof Error-Avoiding Mechanisms\nfor Oxidative DNA Damage in Carcinogenesis","volume":"98","author":"Tsuzuki","year":"2007","journal-title":"Cancer Sci."},{"key":"2026081413075252800_cit6","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/J.DNAREP.2017.09.007","article-title":"Not Breathing\nIs Not an Option: How to Deal with Oxidative DNA Damage","volume":"59","author":"Markkanen","year":"2017","journal-title":"DNA Repair"},{"key":"2026081413075252800_cit7","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1016\/S1568-7864(02)00113-1","article-title":"Mutational\nSpecificity of Mice Defective in the MTH1 and\/or the MSH2 Genes","volume":"1","author":"Egashira","year":"2002","journal-title":"DNA Repair"},{"key":"2026081413075252800_cit8","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.freeradbiomed.2016.11.002","article-title":"Free Radical\nBiology and Medicine\nMTH1 as a Nucleotide Pool Sanitizing Enzyme: Friend or Foe?","volume":"107","author":"Nakabeppu","year":"2017","journal-title":"Free Radical Biol. Med."},{"key":"2026081413075252800_cit9","doi-asserted-by":"publisher","first-page":"1459","DOI":"10.1093\/carcin\/22.9.1459","article-title":"Age-Related\nand Tissue-Specific Accumulation of Oxidative DNA Base\nDamage in 7,8-Dihydro-8-Oxoguanine-DNA Glycosylase (Ogg1) Deficient\nMice","volume":"22","author":"Osterod","year":"2001","journal-title":"Carcinogenesis"},{"key":"2026081413075252800_cit10","doi-asserted-by":"publisher","first-page":"13300","DOI":"10.1073\/pnas.96.23.13300","article-title":"Accumulation of\nPremutagenic DNA Lesions in Mice Defective in Removal of Oxidative\nBase Damage","volume":"96","author":"Klungland","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2026081413075252800_cit11","doi-asserted-by":"publisher","first-page":"1489","DOI":"10.1038\/onc.2010.520","article-title":"Enhanced Elimination of Oxidized\nGuanine Nucleotides Inhibits Oncogenic RAS-Induced DNA Damage and\nPremature Senescence","volume":"30","author":"Rai","year":"2011","journal-title":"Oncogene"},{"key":"2026081413075252800_cit12","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.dnarep.2018.07.006","article-title":"HMTH1 Is Required\nfor Maintaining Migration and Invasion Potential of Human Thyroid\nCancer Cells","volume":"69","author":"Arczewska","year":"2018","journal-title":"DNA Repair"},{"key":"2026081413075252800_cit13","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.ejmech.2019.02.011","article-title":"Discovery\nof a New Class of MTH1\nInhibitor by X-Ray Crystallographic Screening","volume":"167","author":"Yokoyama","year":"2019","journal-title":"Eur. J. Med. Chem."},{"key":"2026081413075252800_cit14","doi-asserted-by":"publisher","first-page":"2533","DOI":"10.1021\/acs.jmedchem.7b01884","article-title":"Creation\nof a Novel\nClass of Potent and Selective MutT Homologue 1 (MTH1) Inhibitors Using\nFragment-Based Screening and Structure-Based Drug Design","volume":"61","author":"Rahm","year":"2018","journal-title":"J. Med. Chem."},{"key":"2026081413075252800_cit15","doi-asserted-by":"publisher","first-page":"8160","DOI":"10.1021\/acs.jmedchem.7b01006","article-title":"Fragment-Based\nDiscovery and Optimization of Enzyme Inhibitors by Docking of Commercial\nChemical Space","volume":"60","author":"Rudling","year":"2017","journal-title":"J. Med. Chem."},{"key":"2026081413075252800_cit16","doi-asserted-by":"publisher","first-page":"862","DOI":"10.1111\/cbdd.12909","article-title":"Identification\nand Structure\u2013Activity Relationship of Purine Derivatives as\nNovel MTH1 Inhibitors","volume":"89","author":"Kumar","year":"2017","journal-title":"Chem. Biol. Drug Des."},{"key":"2026081413075252800_cit17","doi-asserted-by":"publisher","first-page":"1986","DOI":"10.1021\/acschembio.7b00370","article-title":"Novel Class of Potent and Cellularly Active\nInhibitors Devalidates MTH1 as Broad-Spectrum Cancer Target","volume":"12","author":"Ellermann","year":"2017","journal-title":"ACS Chem. Biol."},{"key":"2026081413075252800_cit18","doi-asserted-by":"publisher","first-page":"2346","DOI":"10.1021\/acs.jmedchem.5b01760","article-title":"Potent and Selective Inhibitors of MTH1 Probe\nIts Role in Cancer Cell Survival","volume":"59","author":"Kettle","year":"2016","journal-title":"J. Med. Chem."},{"key":"2026081413075252800_cit19","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1016\/j.bmcl.2016.02.026","article-title":"Identification\nof Potent and Selective MTH1 Inhibitors","volume":"26","author":"Petrocchi","year":"2016","journal-title":"Bioorg.\nMed. Chem. Lett."},{"key":"2026081413075252800_cit20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jpba.2014.11.009","article-title":"Development\nand Validation of Method for TH588 and TH287, Potent MTH1 Inhibitors\nand New Anti-Cancer Agents, for Pharmacokinetic Studies in Mice Plasma","volume":"104","author":"Saleh","year":"2015","journal-title":"J. Pharm. Biomed. Anal."},{"key":"2026081413075252800_cit21","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1038\/nature13194","article-title":"Stereospecific Targeting\nof MTH1 by (S)-Crizotinib as an Anticancer Strategy","volume":"508","author":"Huber","year":"2014","journal-title":"Nature"},{"key":"2026081413075252800_cit22","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1038\/nature13181","article-title":"MTH1 Inhibition Eradicates Cancer by Preventing\nSanitation of the DNTP Pool","volume":"508","author":"Gad","year":"2014","journal-title":"Nature"},{"key":"2026081413075252800_cit23","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1002\/anie.201307849","article-title":"An Organometallic Inhibitor for the\nHuman Repair Enzyme\n7,8-Dihydro-8-Oxoguanosine Triphosphatase","volume":"53","author":"Streib","year":"2014","journal-title":"Angew.\nChem., Int. Ed."},{"key":"2026081413075252800_cit24","doi-asserted-by":"publisher","DOI":"10.3390\/cancers9050047","article-title":"MTH1 as a\nChemotherapeutic Target:\nThe Elephant in the Room","volume":"9","author":"Samaranayake","year":"2017","journal-title":"Cancers"},{"key":"2026081413075252800_cit25","doi-asserted-by":"publisher","first-page":"2334","DOI":"10.1021\/acschembio.5b00452","article-title":"Small Molecule Inhibitors of 8-Oxoguanine\nDNA Glycosylase-1 (OGG1)","volume":"10","author":"Donley","year":"2015","journal-title":"ACS Chem. Biol."},{"key":"2026081413075252800_cit26","doi-asserted-by":"publisher","first-page":"2105","DOI":"10.1021\/jacs.7b09316","article-title":"Potent and Selective\nInhibitors of 8-Oxoguanine DNA\nGlycosylase","volume":"140","author":"Tahara","year":"2018","journal-title":"J. Am. Chem. Soc."},{"key":"2026081413075252800_cit27","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1126\/science.aar8048","article-title":"Small-Molecule\nInhibitor of OGG1 Suppresses Proinflammatory Gene Expression and Inflammation","volume":"362","author":"Visnes","year":"2018","journal-title":"Science"},{"key":"2026081413075252800_cit28","doi-asserted-by":"publisher","first-page":"1329","DOI":"10.1200\/JCO.2006.09.1066","article-title":"Meta-Analysis\nof BRCA1 and BRCA2 Penetrance","volume":"25","author":"Chen","year":"2007","journal-title":"J. Clin. Oncol."},{"key":"2026081413075252800_cit29","doi-asserted-by":"publisher","first-page":"1807","DOI":"10.1053\/j.gastro.2011.01.057","article-title":"Intestinal Inflammation and Cancer","volume":"140","author":"Ullman","year":"2011","journal-title":"Gastroenterology"},{"key":"2026081413075252800_cit30","doi-asserted-by":"publisher","first-page":"3937","DOI":"10.3748\/wjg.14.3937","article-title":"Risk for Colorectal Cancer in Ulcerative Colitis: Changes,\nCauses and Management Strategies","volume":"14","author":"Lakatos","year":"2008","journal-title":"World J. Gastroenterol."},{"key":"2026081413075252800_cit31","doi-asserted-by":"publisher","first-page":"6205","DOI":"10.1158\/0008-5472.CAN-14-1716","article-title":"Therapeutic\nTargeting\nof Brca1-Mutated Breast Cancers with Agents That Activate Dna Repair","volume":"74","author":"Alli","year":"2014","journal-title":"Cancer Res."},{"key":"2026081413075252800_cit32","doi-asserted-by":"publisher","DOI":"10.4161\/23723556.2014.979685","article-title":"BRCA1: A Movement\ntoward Cancer Prevention","volume":"2","author":"Alli","year":"2015","journal-title":"Mol. Cell. Oncol."},{"key":"2026081413075252800_cit33","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.freeradbiomed.2018.05.094","article-title":"Enhanced Mitochondrial\nDNA Repair of the Common Disease-Associated\nVariant, Ser326Cys, of HOGG1 through Small Molecule Intervention","volume":"124","author":"Baptiste","year":"2018","journal-title":"Free Radical Biol. Med."},{"key":"2026081413075252800_cit34","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1128\/mcb.24.1.465-474.2004","article-title":"The Oxidized Deoxynucleoside\nTriphosphate Pool Is a Significant Contributor to Genetic Instability\nin Mismatch Repair-Deficient Cells","volume":"24","author":"Russo","year":"2004","journal-title":"Mol. Cell.\nBiol."},{"key":"2026081413075252800_cit35","doi-asserted-by":"publisher","first-page":"9005","DOI":"10.1021\/jacs.6b02895","article-title":"A Chimeric ATP-Linked\nNucleotide Enables Luminescence Signaling of Damage Surveillance by\nMTH1, a Cancer Target","volume":"138","author":"Ji","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"2026081413075252800_cit36","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/0022-5193(76)90059-X","article-title":"The Theoretical\nAnalysis of Kinetic Behaviour of \u201cHysteretic\u201d Allosteric\nEnzymes. I. The Kinetic Manifestations of Slow Conformational Change\nof an Oligomeric Enyzme in the Monod, Wyman and Changeux Model","volume":"60","author":"Kurganov","year":"1976","journal-title":"J. Theor. Biol."},{"key":"2026081413075252800_cit37","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1111\/j.1432-1033.1972.tb01746.x","article-title":"Kinetic Study of the Activation Process\nof \u03b2-Galactosidase From Escherichia Coli by Mg2+","volume":"26","author":"Tenu","year":"1972","journal-title":"Eur. J. Biochem."},{"key":"2026081413075252800_cit38","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/j.addr.2012.09.019","article-title":"Experimental and\nComputational Approaches to Estimate Solubility and Permeability in\nDrug Discovery and Development Settings","volume":"64","author":"Lipinski","year":"2012","journal-title":"Adv.\nDrug Delivery Rev."},{"key":"2026081413075252800_cit39","doi-asserted-by":"publisher","first-page":"4564","DOI":"10.1016\/j.bmc.2012.05.047","article-title":"Abbott Physicochemical\nTiering (APT)\n- A Unified Approach to HTS Triage","volume":"20","author":"Cox","year":"2012","journal-title":"Bioorg.\nMed. Chem."},{"key":"2026081413075252800_cit40","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1111\/gtc.12022","article-title":"Activity-Based Kinase\nProfiling of Approved Tyrosine Kinase Inhibitors","volume":"18","author":"Kitagawa","year":"2013","journal-title":"Genes Cells"},{"key":"2026081413075252800_cit41","doi-asserted-by":"publisher","first-page":"4701","DOI":"10.1021\/jm100395q","article-title":"Discovery of 3-[2-(Imidazo\u00ad[1,2- b]\u00adPyridazin-3-Yl)\u00adEthynyl]-4-Methyl- N -{4-[(4-Methylpiperazin-1-Yl)\u00adMethyl]-3-(Trifluoromethyl)\u00adPhenyl}\u00adbenzamide\n(AP24534), a Potent, Orally Active Pan-Inhibitor of Breakpoint Cluster\nRegion-Abelson (BCR-ABL) Kinase Including the T315I Gatekeeper Mutant","volume":"53","author":"Huang","year":"2010","journal-title":"J. Med. Chem."},{"key":"2026081413075252800_cit42","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0092146","article-title":"Comparison of\nthe Cancer Gene Targeting and Biochemical Selectivities of All Targeted\nKinase Inhibitors Approved for Clinical Use","volume":"9","author":"Uitdehaag","year":"2014","journal-title":"PLoS One"},{"key":"2026081413075252800_cit43","doi-asserted-by":"publisher","DOI":"10.1186\/s12943-018-0804-2","article-title":"Kinase-Targeted Cancer Therapies:\nProgress, Challenges and Future Directions","volume":"17","author":"Bhullar","year":"2018","journal-title":"Mol. 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Pharm. Sci."},{"key":"2026081413075252800_cit47","doi-asserted-by":"publisher","first-page":"1490","DOI":"10.1023\/a:1011930411574","article-title":"Correlating Partitioning\nand Caco-2 Cell Permeability of Structurally Diverse Small Molecule\nWeight Compounds","volume":"15","author":"Yazdanian","year":"1998","journal-title":"Pharm. Res."},{"key":"2026081413075252800_cit48","doi-asserted-by":"publisher","first-page":"1497","DOI":"10.1124\/dmd.30.12.1497","article-title":"The Influence\nof Nonspecific Microsomal Binding on Apparent Intrinsic Clearance,\nand Its Prediction from Physicochemical Properties","volume":"30","author":"Austin","year":"2002","journal-title":"Drug Metab. 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Technol."},{"key":"2026081413075252800_cit51","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0151154","article-title":"MTH1 Substrate Recognition-An Example\nof Specific Promiscuity","volume":"11","author":"Nissink","year":"2016","journal-title":"PLoS One"},{"key":"2026081413075252800_cit52","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1016\/j.bbabio.2006.02.010","article-title":"Mitochondrial\nMetabolic States Regulate Nitric Oxide and Hydrogen Peroxide Diffusion\nto the Cytosol","volume":"1757","author":"Boveris","year":"2006","journal-title":"Biochim. Biophys. Acta, Bioenerg."},{"key":"2026081413075252800_cit53","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.mrgentox.2008.09.017","article-title":"Oxidative\nStress in Environmental-Induced\nCarcinogenesis","volume":"674","author":"Mena","year":"2009","journal-title":"Mutat. Res., Genet. Toxicol.\nEnviron. 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