DNA double-strand breaks (DSBs) are mainly repaired by c-NHEJ and HR pathways. The enhanced DSB mobility after DNA damage is critical for efficient DSB repair. Although microtubule dynamics have been shown to regulate DSB mobility, the reverse effect of DSBs to microtubule dynamics remains elusive. Here, we uncovered a novel DSB-induced microtubule dynamics stress response (DMSR), which promotes DSB mobility and facilitates c-NHEJ repair. DMSR is accompanied by interphase centrosome maturation, which occurs in a DNA-PK-AKT–dependent manner. Depletion of PCM proteins attenuates DMSR and the mobility of DSBs, resulting in delayed c-NHEJ. Remarkably, DMSR occurs only in G1 or G0 cells and lasts around 6 h. Both inhibition of DNA-PK and depletion of 53BP1 abolish DMSR. Taken together, our study reveals a positive DNA repair mechanism in G1 or G0 cells in which DSBs actively promote microtubule dynamics and facilitate the c-NHEJ process.
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January 06 2021
DNA damage promotes microtubule dynamics through a DNA-PK-AKT axis for enhanced repair
Shuyun Ma,
Shuyun Ma
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
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Zeming Rong,
Zeming Rong
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
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Chen Liu,
Chen Liu
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
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Xiaobing Qin,
Xiaobing Qin
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
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Xiaoyan Zhang,
Xiaoyan Zhang
3
College of Biomedicine and Health, Huazhong Agricultural University, Wuhan, China
4
College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
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Qiang Chen
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Correspondence to Qiang Chen: C52616@hotmail.com
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Shuyun Ma
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Zeming Rong
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Chen Liu
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Xiaobing Qin
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Xiaoyan Zhang
3
College of Biomedicine and Health, Huazhong Agricultural University, Wuhan, China
4
College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
Qiang Chen
1
Department of Radiation and Medical Oncology, Medical Research Institute, Zhongnan Hospital of Wuhan University, Wuhan University, Wuhan, China
2
Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, Wuhan, China
Correspondence to Qiang Chen: C52616@hotmail.com
Received:
November 06 2019
Revision Received:
November 01 2020
Accepted:
December 02 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
National Basic Research Program of China (973 Program)
(2018YFC1003400)
National Natural Science Foundation of China
(31770868)
Wuhan University
(2042018kf0215)
© 2020 Ma et al.
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2021) 220 (2): e201911025.
Article history
Received:
November 06 2019
Revision Received:
November 01 2020
Accepted:
December 02 2020
Citation
Shuyun Ma, Zeming Rong, Chen Liu, Xiaobing Qin, Xiaoyan Zhang, Qiang Chen; DNA damage promotes microtubule dynamics through a DNA-PK-AKT axis for enhanced repair. J Cell Biol 1 February 2021; 220 (2): e201911025. doi: https://doi.org/10.1083/jcb.201911025
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