Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene

Abstract Numerous chemicals are associated with carcinogenesis through epigenetic alterations in cells. To detect global epigenetic changes induced by carcinogens, the housekeeping gene can serve as a reporter locus, offering a baseline for identifying shifts in epigenetic marks. To investigate this...

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Main Authors: Haruto Yamada, Mizuki Odagiri, Keigo Yamakita, Aoi Chiba, Akiko Ukai, Manabu Yasui, Masamitsu Honma, Kei-ichi Sugiyama, Kiyoe Ura, Akira Sassa
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-92121-6
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author Haruto Yamada
Mizuki Odagiri
Keigo Yamakita
Aoi Chiba
Akiko Ukai
Manabu Yasui
Masamitsu Honma
Kei-ichi Sugiyama
Kiyoe Ura
Akira Sassa
author_facet Haruto Yamada
Mizuki Odagiri
Keigo Yamakita
Aoi Chiba
Akiko Ukai
Manabu Yasui
Masamitsu Honma
Kei-ichi Sugiyama
Kiyoe Ura
Akira Sassa
author_sort Haruto Yamada
collection DOAJ
description Abstract Numerous chemicals are associated with carcinogenesis through epigenetic alterations in cells. To detect global epigenetic changes induced by carcinogens, the housekeeping gene can serve as a reporter locus, offering a baseline for identifying shifts in epigenetic marks. To investigate this potential, we developed a simple, cost-effective, and quantitative reporter system to assess chemically induced epigenetic effects, utilizing the thymidine kinase (TK) gene mutation assay as a foundation. Using a standard genotoxicity test cell line, human lymphoblast TK6, we edited the CpG promoter loci of the endogenous TK gene using the CRISPR/dCas9-SunTag-DNMT3A system. This epi-genotoxicity assay, employing modified mTK6 cells, provides a simple method for quantifying chemically induced epigenetic effects. The assay successfully detects both increased TK reversion rates induced by DNMT inhibitors, such as 5-Aza-2′-deoxycytidine and GSK-3484862, and, for the first time, a significant reduction in TK revertant frequency caused by the non-genotoxic carcinogen 12-O-tetradecanoylphorbol-13-acetate (TPA). Chromatin immunoprecipitation and western blotting analyses revealed that TPA treatment led to a global decrease in H3K27Ac levels, likely driven by TPA-mediated inflammation. These results demonstrate the utility of the epi-genotoxicity assay as a valuable tool for evaluating dual-directional epigenetic changes triggered by chemical exposure.
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spelling doaj-art-12974871e88949fa97bc16fd187005dd2025-08-20T02:59:24ZengNature PortfolioScientific Reports2045-23222025-03-0115111210.1038/s41598-025-92121-6Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK geneHaruto Yamada0Mizuki Odagiri1Keigo Yamakita2Aoi Chiba3Akiko Ukai4Manabu Yasui5Masamitsu Honma6Kei-ichi Sugiyama7Kiyoe Ura8Akira Sassa9Department of Biology, Graduate School of Science, Chiba UniversityDepartment of Biology, Graduate School of Science, Chiba UniversityDepartment of Biology, Graduate School of Science, Chiba UniversityDepartment of Biology, Graduate School of Science, Chiba UniversityDivision of Genome Safety Science, National Institute of Health SciencesDivision of Genome Safety Science, National Institute of Health SciencesDivision of Genome Safety Science, National Institute of Health SciencesDivision of Genome Safety Science, National Institute of Health SciencesDepartment of Biology, Graduate School of Science, Chiba UniversityDepartment of Biology, Graduate School of Science, Chiba UniversityAbstract Numerous chemicals are associated with carcinogenesis through epigenetic alterations in cells. To detect global epigenetic changes induced by carcinogens, the housekeeping gene can serve as a reporter locus, offering a baseline for identifying shifts in epigenetic marks. To investigate this potential, we developed a simple, cost-effective, and quantitative reporter system to assess chemically induced epigenetic effects, utilizing the thymidine kinase (TK) gene mutation assay as a foundation. Using a standard genotoxicity test cell line, human lymphoblast TK6, we edited the CpG promoter loci of the endogenous TK gene using the CRISPR/dCas9-SunTag-DNMT3A system. This epi-genotoxicity assay, employing modified mTK6 cells, provides a simple method for quantifying chemically induced epigenetic effects. The assay successfully detects both increased TK reversion rates induced by DNMT inhibitors, such as 5-Aza-2′-deoxycytidine and GSK-3484862, and, for the first time, a significant reduction in TK revertant frequency caused by the non-genotoxic carcinogen 12-O-tetradecanoylphorbol-13-acetate (TPA). Chromatin immunoprecipitation and western blotting analyses revealed that TPA treatment led to a global decrease in H3K27Ac levels, likely driven by TPA-mediated inflammation. These results demonstrate the utility of the epi-genotoxicity assay as a valuable tool for evaluating dual-directional epigenetic changes triggered by chemical exposure.https://doi.org/10.1038/s41598-025-92121-6ToxicologyEpi-genotoxicityReporter assay12-O-tetradecanoylphorbol-13-acetateDNMT inhibitorTK gene
spellingShingle Haruto Yamada
Mizuki Odagiri
Keigo Yamakita
Aoi Chiba
Akiko Ukai
Manabu Yasui
Masamitsu Honma
Kei-ichi Sugiyama
Kiyoe Ura
Akira Sassa
Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
Scientific Reports
Toxicology
Epi-genotoxicity
Reporter assay
12-O-tetradecanoylphorbol-13-acetate
DNMT inhibitor
TK gene
title Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
title_full Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
title_fullStr Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
title_full_unstemmed Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
title_short Dual-directional epi-genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping TK gene
title_sort dual directional epi genotoxicity assay for assessing chemically induced epigenetic effects utilizing the housekeeping tk gene
topic Toxicology
Epi-genotoxicity
Reporter assay
12-O-tetradecanoylphorbol-13-acetate
DNMT inhibitor
TK gene
url https://doi.org/10.1038/s41598-025-92121-6
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