Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin

Abstract Background Bleomycin (Bleo) is a glycopeptide with potent antitumor activity that induces DNA double-strand breaks (DSBs) through free radical generation, similar to ionizing radiation (IR). Therefore, Bleo is considered a radiomimetic drug. However, differences in DNA repair mechanisms bet...

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Main Authors: Naoto Shimizu, Kazuki Izawa, Mubasshir Washif, Ryosuke Morozumi, Kouji Hirota, Masataka Tsuda
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Genes and Environment
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Online Access:https://doi.org/10.1186/s41021-025-00329-9
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author Naoto Shimizu
Kazuki Izawa
Mubasshir Washif
Ryosuke Morozumi
Kouji Hirota
Masataka Tsuda
author_facet Naoto Shimizu
Kazuki Izawa
Mubasshir Washif
Ryosuke Morozumi
Kouji Hirota
Masataka Tsuda
author_sort Naoto Shimizu
collection DOAJ
description Abstract Background Bleomycin (Bleo) is a glycopeptide with potent antitumor activity that induces DNA double-strand breaks (DSBs) through free radical generation, similar to ionizing radiation (IR). Therefore, Bleo is considered a radiomimetic drug. However, differences in DNA repair mechanisms between IR- and Bleo-induced DNA damage have not been fully elucidated. Therefore, in the present study, we examined a panel of repair-deficient human TK6 cell lines to elucidate the relative contributions of individual repair factors. Results Our comprehensive profiling indicated that both non-homologous end joining (NHEJ) and homologous recombination (HR) contributed to DSB repair induced by X-rays and Bleo. Furthermore, tyrosyl-DNA phosphodiesterase (TDP)-related repair was a significant factor for cellular sensitivity to Bleo treatment. TDP1 −/− /TDP2 −/− cells exhibited greater sensitivity to Bleo than TDP1 −/− or TDP2 −/− cells, but not to X-rays. In addition, we determined whether TDP2 is involved in the repair of Bleo-induced DSBs using a neutral comet assay. In TDP1-deficient cells, knockout of TDP2 resulted in a significant delay in the repair kinetics of DSBs induced by Bleo, but not by X-rays. Conclusions The contribution of the TDP-related pathway to DSB repair significantly differed between IR and radiomimetic drugs. The discovery of this novel TDP2-dependent repair of DSBs resulting from radiomimetic drug exposure indicates that TDP1 and TDP2 inhibition in combination with radiomimetic drugs represents a strategy for cancer treatment.
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spelling doaj-art-8e6b8aff2dda4e988b1db19d7b45991a2025-08-20T03:40:48ZengBMCGenes and Environment1880-70622025-03-0147111010.1186/s41021-025-00329-9Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug BleomycinNaoto Shimizu0Kazuki Izawa1Mubasshir Washif2Ryosuke Morozumi3Kouji Hirota4Masataka Tsuda5Program of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima UniversityDivision of Genome Safety Science, National Institute of Health SciencesDepartment of Chemistry, Graduate School of Science, Tokyo Metropolitan UniversityProgram of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima UniversityDepartment of Chemistry, Graduate School of Science, Tokyo Metropolitan UniversityProgram of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima UniversityAbstract Background Bleomycin (Bleo) is a glycopeptide with potent antitumor activity that induces DNA double-strand breaks (DSBs) through free radical generation, similar to ionizing radiation (IR). Therefore, Bleo is considered a radiomimetic drug. However, differences in DNA repair mechanisms between IR- and Bleo-induced DNA damage have not been fully elucidated. Therefore, in the present study, we examined a panel of repair-deficient human TK6 cell lines to elucidate the relative contributions of individual repair factors. Results Our comprehensive profiling indicated that both non-homologous end joining (NHEJ) and homologous recombination (HR) contributed to DSB repair induced by X-rays and Bleo. Furthermore, tyrosyl-DNA phosphodiesterase (TDP)-related repair was a significant factor for cellular sensitivity to Bleo treatment. TDP1 −/− /TDP2 −/− cells exhibited greater sensitivity to Bleo than TDP1 −/− or TDP2 −/− cells, but not to X-rays. In addition, we determined whether TDP2 is involved in the repair of Bleo-induced DSBs using a neutral comet assay. In TDP1-deficient cells, knockout of TDP2 resulted in a significant delay in the repair kinetics of DSBs induced by Bleo, but not by X-rays. Conclusions The contribution of the TDP-related pathway to DSB repair significantly differed between IR and radiomimetic drugs. The discovery of this novel TDP2-dependent repair of DSBs resulting from radiomimetic drug exposure indicates that TDP1 and TDP2 inhibition in combination with radiomimetic drugs represents a strategy for cancer treatment.https://doi.org/10.1186/s41021-025-00329-9Radiomimetic drugsBleomycinIonizing radiationDNA double-strand breaksTK6Tyrosyl-DNA phosphodiesterase
spellingShingle Naoto Shimizu
Kazuki Izawa
Mubasshir Washif
Ryosuke Morozumi
Kouji Hirota
Masataka Tsuda
Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
Genes and Environment
Radiomimetic drugs
Bleomycin
Ionizing radiation
DNA double-strand breaks
TK6
Tyrosyl-DNA phosphodiesterase
title Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
title_full Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
title_fullStr Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
title_full_unstemmed Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
title_short Role of TDP2 in the repair of DNA damage induced by the radiomimetic drug Bleomycin
title_sort role of tdp2 in the repair of dna damage induced by the radiomimetic drug bleomycin
topic Radiomimetic drugs
Bleomycin
Ionizing radiation
DNA double-strand breaks
TK6
Tyrosyl-DNA phosphodiesterase
url https://doi.org/10.1186/s41021-025-00329-9
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