Abstract
Purpose
The transcription factor NF-E2-related factor 2 (NRF2) is a master regulator widely involved in essential cellular functions such as DNA repair. By clarifying the upstream and downstream links of NRF2 to DNA damage repair, we hope that attention will be drawn to the utilization of NRF2 as a target for cancer therapy.
Methods
Query and summarize relevant literature on the role of NRF2 in direct repair, BER, NER, MMR, HR, and NHEJ in pubmed. Make pictures of Roles of NRF2 in DNA Damage Repair and tables of antioxidant response elements (AREs) of DNA repair genes. Analyze the mutation frequency of NFE2L2 in different types of cancer using cBioPortal online tools. By using TCGA, GTEx and GO databases, analyze the correlation between NFE2L2 mutations and DNA repair systems as well as the degree of changes in DNA repair systems as malignant tumors progress.
Results
NRF2 plays roles in maintaining the integrity of the genome by repairing DNA damage, regulating the cell cycle, and acting as an antioxidant. And, it possibly plays roles in double stranded break (DSB) pathway selection following ionizing radiation (IR) damage. Whether pathways such as RNA modification, ncRNA, and protein post-translational modification affect the regulation of NRF2 on DNA repair is still to be determined. The overall mutation frequency of the NFE2L2 gene in esophageal carcinoma, lung cancer, and penile cancer is the highest. Genes (50 of 58) that are negatively correlated with clinical staging are positively correlated with NFE2L2 mutations or NFE2L2 expression levels.
Conclusion
NRF2 participates in a variety of DNA repair pathways and plays important roles in maintaining genome stability. NRF2 is a potential target for cancer treatment.
Similar content being viewed by others
Data Availability
Not applicable.
References
J.F. Alhmoud, J.F. Woolley, A.E. Al Moustafa, M.I. Malki, DNA Damage/Repair management in cancers. Cancers (Basel). 12, (2020)
C.K. Davis, R. Vemuganti, DNA damage and repair following traumatic brain injury. Neurobiol. Dis. 147, 105143 (2021)
U.S. Srinivas, B.W.Q. Tan, B.A. Vellayappan, A.D. Jeyasekharan, ROS and the DNA damage response in cancer. Redox Biol. 25, 101084 (2019)
N. Chatterjee, G.C. Walker, Mechanisms of DNA damage, repair, and mutagenesis. Environ. Mol. Mutagen. 58, 235–263 (2017)
K.R. Sekhar, M.L. Freeman, Nrf2 promotes survival following exposure to ionizing radiation. Free Radic Biol Med. 88, 268–274 (2015)
M. Rojo, de la E. Vega, D.D. Chapman, Zhang, NRF2 and the Hallmarks of Cancer. Cancer Cell. 34, 21–43 (2018)
D.D. Zhang, E. Chapman, The role of natural products in revealing NRF2 function. Nat. Prod. Rep. 37, 797–826 (2020)
K. Taguchi, M. Yamamoto, The KEAP1-NRF2 system in Cancer. Front. Oncol. 7, 85 (2017)
M. Anuranjani, Bala, Concerted action of Nrf2-ARE pathway, MRN complex, HMGB1 and inflammatory cytokines - implication in modification of radiation damage. Redox Biol. 2, 832–846 (2014)
X. Sun, Y. Wang, K. Ji, Y. Liu, Y. Kong, S. Nie, N. Li, J. Hao, Y. Xie, C. Xu, L. Du, Q. Liu, NRF2 preserves genomic integrity by facilitating ATR activation and G2 cell cycle arrest. Nucleic Acids Res. 48, 9109–9123 (2020)
L. Yang, C. Shen, A. Estrada-Bernal, R. Robb, M. Chatterjee, N. Sebastian, A. Webb, X. Mo, W. Chen, S. Krishnan, T.M. Williams, Oncogenic KRAS drives radioresistance through upregulation of NRF2-53BP1-mediated non-homologous end-joining repair. Nucleic Acids Res. 49, 11067–11082 (2021)
H. Zhao, L. Song, N. Ma, C. Liu, Y. Dun, Z. Zhou, D. Yuan, C. Zhang, The dynamic changes of Nrf2 mediated oxidative stress, DNA damage and base excision repair in testis of rats during aging. Exp. Gerontol. 152, 111460 (2021)
D.K. Sah, Y. Rai, A. Chauhan, N. Kumari, M.M. Chaturvedi, A.N. Bhatt, Sphingosine kinase inhibitor, SKI-II confers protection against the ionizing radiation by maintaining redox homeostasis most likely through Nrf2 signaling. Life Sci. 278, 119543 (2021)
T. Gruosso, V. Mieulet, M. Cardon, B. Bourachot, Y. Kieffer, F. Devun, T. Dubois, M. Dutreix, A. Vincent-Salomon, K.M. Miller, F. Mechta-Grigoriou, Chronic oxidative stress promotes H2AX protein degradation and enhances chemosensitivity in breast cancer patients. EMBO Mol. Med. 8, 527–549 (2016)
F. He, X. Ru, T. Wen, NRF2, a transcription factor for stress response and Beyond. Int. J. Mol. Sci. 21, (2020)
B. Chen, Y. Zhang, Y. Wang, J. Rao, X. Jiang, Z. Xu, Curcumin inhibits proliferation of breast cancer cells through Nrf2-mediated down-regulation of Fen1 expression. J. Steroid Biochem. Mol. Biol. 143, 11 – 8 (2014)
N. Duru, R. Gernapudi, Y. Zhang, Y. Yao, P.K. Lo, B. Wolfson, Q. Zhou, NRF2/miR-140 signaling confers radioprotection to human lung fibroblasts. Cancer Lett. 369, 184–191 (2015)
M.A. Ibrahim Al-Obaide, V. Arutla, M.D. Bacolod, W. Wang, R. Zhang, K.S. Srivenugopal, Genomic space of MGMT in Human Glioma Revisited: Novel Motifs, Regulatory RNAs, NRF1, 2, and CTCF involvement in Gene expression. Int. J. Mol. Sci. 22, (2021)
E. Zgorzynska, B. Dziedzic, A. Walczewska, An overview of the Nrf2/ARE pathway and its role in neurodegenerative Diseases. Int. J. Mol. Sci. 22, (2021)
G. Chevillard, V. Blank, NFE2L3 (NRF, The Cinderella of the Cap’n’collar transcription factors. Cell. Mol. Life Sci. 68(3), 3337–3348 (2011)
W. Han, M. Ming, R. Zhao, J. Pi, C. Wu, Y.Y. He, Nrf1 CNC-bZIP protein promotes cell survival and nucleotide excision repair through maintaining glutathione homeostasis. J. Biol. Chem. 287, 18788–18795 (2012)
C. Yi, C. He, DNA repair by reversal of DNA damage. Cold Spring Harb. Perspect. Biol. 5, a012575 (2013)
T. Iyama, D.M. 3 Wilson, rd, DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst). 12, 620 – 36 (2013)
H. Xu, J. Jin, Y. Chen, G. Wu, H. Zhu, Q. Wang, J. Wang, S. Li, F.N. Grigore, J. Ma, C.C. Chen, Q. Lan, M. Li, GBP3 promotes glioblastoma resistance to temozolomide by enhancing DNA damage repair. Oncogene. 41, 3876–3885 (2022)
R. Meas, J.J. Wyrick, M.J. Smerdon, Nucleosomes regulate base excision repair in chromatin. Mutat. Res. Rev. Mutat. Res. 780, 29–36 (2019)
W. Li, K. Jones, T.J. Burke, M.A. Hossain, L. Lariscy, Epigenetic regulation of Nucleotide Excision Repair. Front. Cell. Dev. Biol. 10, 847051 (2022)
K.J. Wozniak, L.A. Simmons, Bacterial DNA excision repair pathways. Nat. Rev. Microbiol. 20, 465–477 (2022)
S.L. Habib, A. Yadav, D. Kidane, R.H. Weiss, S. Liang, Novel protective mechanism of reducing renal cell damage in diabetes: activation AMPK by AICAR increased NRF2/OGG1 proteins and reduced oxidative DNA damage. Cell. Cycle. 15, 3048–3059 (2016)
C.M. Harris, K.E. Zamperoni, S.C. Sernoskie, N.S.M. Chow, T.E. Massey, Effects of in vivo treatment of mice with sulforaphane on repair of DNA pyridyloxylbutylation. Toxicology. 454, 152753 (2021)
P. Liu, D. Ma, P. Wang, C. Pan, Q. Fang, J. Wang, Nrf2 overexpression increases risk of high tumor mutation burden in acute myeloid leukemia by inhibiting MSH2. Cell. Death Dis. 12, 20 (2021)
G.J. Grundy, J.L. Parsons, Base excision repair and its implications to cancer therapy. Essays Biochem. 64, 831–843 (2020)
E. Madders, J.L. Parsons, Base excision repair in chromatin and the requirement for chromatin remodelling. Adv. Exp. Med. Biol. 1241, 59–75 (2020)
X. Ma, H. Ming, L. Liu, J. Zhu, L. Pan, Y. Chen, Y. Xiang, OGG1 in lung-more than Base Excision Repair. Antioxid. (Basel). 11, (2022)
K.C. Kim, I.K. Lee, K.A. Kang, J.W. Cha, S.J. Cho, S.Y. Na, S. Chae, H.S. Kim, S. Kim, J.W. Hyun, 7,8-Dihydroxyflavone suppresses oxidative stress-induced base modification in DNA via induction of the repair enzyme 8-oxoguanine DNA glycosylase-1. Biomed. Res. Int. 2013, 863720 (2013)
K.J. Rodriguez, H.K. Wong, T. Oddos, M. Southall, B. Frei, S. Kaur, A purified feverfew extract protects from oxidative damage by inducing DNA repair in skin cells via a PI3-kinase-dependent Nrf2/ARE pathway. J. Dermatol. Sci. 72, 304–310 (2013)
B. Singh, A. Chatterjee, A.M. Ronghe, N.K. Bhat, H.K. Bhat, Antioxidant-mediated up-regulation of OGG1 via NRF2 induction is associated with inhibition of oxidative DNA damage in estrogen-induced breast cancer. BMC Cancer. 13, 253 (2013)
L. Balakrishnan, R.A. Bambara, Flap endonuclease 1. Annu. Rev. Biochem. 82, 119 – 38 (2013)
X. Lu, R. Liu, M. Wang, A.K. Kumar, F. Pan, L. He, Z. Hu, Z. Guo, MicroRNA-140 impedes DNA repair by targeting FEN1 and enhances chemotherapeutic response in breast cancer. Oncogene. 39, 234–247 (2020)
J.A. Marteijn, H. Lans, W. Vermeulen, J.H. Hoeijmakers, Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell. Biol. 15, 465–481 (2014)
G. Spivak, Nucleotide excision repair in humans. DNA Repair. (Amst). 36, 13–18 (2015)
X. Zhang, M. Yin, J. Hu, Nucleotide excision repair: a versatile and smart toolkit. Acta Biochim. Biophys. Sin (Shanghai). 54, 807–819 (2022)
S. Wei, T. Li, R. Xie, B. Ye, J. Xiang, K. Liu, Z. Chen, X. Gao, The role of ATF3 in ZnO nanoparticle-induced genotoxicity and cytotoxicity in bronchial epithelial cells. Int. J. Biochem. Cell. Biol. 113, 95–102 (2019)
H. Cui, X. Li, C. Han, Q.E. Wang, H. Wang, H.F. Ding, J. Zhang, C. Yan, The stress-responsive gene ATF3 mediates dichotomous UV responses by regulating the Tip60 and p53 proteins. J. Biol. Chem. 291, 10847–10857 (2016)
M. Baretti, D.T. Le, DNA mismatch repair in cancer. Pharmacol. Ther. 189, 45–62 (2018)
L.Y. Kadyrova, F.A. Kadyrov, Endonuclease activities of MutLalpha and its homologs in DNA mismatch repair. DNA Repair. (Amst). 38, 42–49 (2016)
Y. Huang, G.M. Li, DNA mismatch repair in the chromatin context: mechanisms and therapeutic potential. DNA Repair. (Amst). 93, 102918 (2020)
Z.W. Kockler, B. Osia, R. Lee, K. Musmaker, A. Malkova, Repair of DNA breaks by Break-Induced replication. Annu. Rev. Biochem. 90, 165–191 (2021)
R. Ceccaldi, B. Rondinelli, A.D. D’Andrea, Repair pathway choices and consequences at the double-strand break. Trends Cell. Biol. 26, 52–64 (2016)
A.N. Blackford, S.P. Jackson, A.T.M. ATR, The trinity at the heart of the DNA damage response. Mol. Cell. 66, 801–817 (2017)
R. Scully, A. Panday, R. Elango, N.A. Willis, DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat. Rev. Mol. Cell. Biol. 20, 698–714 (2019)
A. Kinner, W. Wu, C. Staudt, G. Iliakis, Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36, 5678–5694 (2008)
M.S. Gilardini Montani, G. Tarquini, R. Santarelli, R. Gonnella, M.A. Romeo, R. Benedetti, A. Arena, A. Faggioni, M. Cirone, p62/SQSTM1 promotes mitophagy and activates the NRF2-mediated antioxidant and anti-inflammatory response restraining EBV-driven B lymphocyte proliferation. Carcinogenesis. 43, 277–287 (2022)
A. Georgoulis, C.E. Vorgias, G.P. Chrousos, E.P. Rogakou, Genome instability and gammaH2AX. Int. J. Mol. Sci. 18, (2017)
W.D. Wright, S.S. Shah, W.D. Heyer, Homologous recombination and the repair of DNA double-strand breaks. J. Biol. Chem. 293, 10524–10535 (2018)
N. Hustedt, D. Durocher, The control of DNA repair by the cell cycle. Nat. Cell. Biol. 19, 1–9 (2016)
S. Jayakumar, D. Pal, S.K. Sandur, Nrf2 facilitates repair of radiation induced DNA damage through homologous recombination repair pathway in a ROS independent manner in cancer cells. Mutat. Res. 779, 33–45 (2015)
A. You, C.W. Nam, N. Wakabayashi, M. Yamamoto, T.W. Kensler, M.K. Kwak, Transcription factor Nrf2 maintains the basal expression of Mdm2: an implication of the regulation of p53 signaling by Nrf2. Arch. Biochem. Biophys. 507, 356–364 (2011)
S.B. Kim, R.K. Pandita, U. Eskiocak, P. Ly, A. Kaisani, R. Kumar, C. Cornelius, W.E. Wright, T.K. Pandita, J.W. Shay, Targeting of Nrf2 induces DNA damage signaling and protects colonic epithelial cells from ionizing radiation. Proc. Natl. Acad. Sci. U S A 109, E2949–E2955 (2012)
D. Lastra, M. Escoll, A. Cuadrado, Transcription factor NRF2 participates in cell cycle progression at the level of G1/S and mitotic checkpoints. Antioxid. (Basel). 11, (2022)
M. Herok, B. Wawrzynow, M.J. Maluszek, M.B. Olszewski, A. Zylicz, M. Zylicz, Chemotherapy of HER2- and MDM2-Enriched breast Cancer subtypes induces homologous recombination DNA repair and chemoresistance. Cancers (Basel). 13, (2021)
X. Sun, M. Dong, Y. Gao, Y. Wang, L. Du, Y. Liu, Q. Wang, K. Ji, N. He, J. Wang, M. Zhang, Y. Gu, H. Song, H. Zhai, L. Feng, C. Xu, Q. Liu, Metformin increases the radiosensitivity of non-small cell lung cancer cells by destabilizing NRF2. Biochem. Pharmacol. 199, 114981 (2022)
Z. Chen, X. Wang, T. Jin, Y. Wang, C.S. Hong, L. Tan, T. Dai, L. Wu, Z. Zhuang, C. Shi, Increase in the radioresistance of normal skin fibroblasts but not tumor cells by mechanical injury. Cell. Death Dis. 8, e2573 (2017)
B. Zhao, E. Rothenberg, D.A. Ramsden, M.R. Lieber, The molecular basis and disease relevance of non-homologous DNA end joining. Nat. Rev. Mol. Cell. Biol. 21, 765–781 (2020)
S.K. Radhakrishnan, N. Jette, S.P. Lees-Miller, Non-homologous end joining: emerging themes and unanswered questions. DNA Repair. (Amst). 17, 2–8 (2014)
K. Yang, R. Guo, D. Xu, Non-homologous end joining: advances and frontiers. Acta Biochim. Biophys. Sin (Shanghai). 48, 632–640 (2016)
H.H.Y. Chang, N.R. Pannunzio, N. Adachi, M.R. Lieber, Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat. Rev. Mol. Cell. Biol. 18, 495–506 (2017)
S. Qin, X. He, H. Lin, B.A. Schulte, M. Zhao, K.D. Tew, G.Y. Wang, Nrf2 inhibition sensitizes breast cancer stem cells to ionizing radiation via suppressing DNA repair. Free Radic Biol Med. 169, 238–247 (2021)
S.S. Deville, S. Luft, M. Kaufmann, N. Cordes, Keap1 inhibition sensitizes head and neck squamous cell carcinoma cells to ionizing radiation via impaired non-homologous end joining and induced autophagy. Cell. Death Dis. 11, 887 (2020)
Q. Wang, J. Li, X. Yang, H. Sun, S. Gao, H. Zhu, J. Wu, W. Jin, Nrf2 is associated with the regulation of basal transcription activity of the BRCA1 gene. Acta. Biochim. Biophys. Sin. (Shanghai). 45, 179 – 87 (2013)
P. Xu, Q. Liu, Y. Xie, X. Shi, Y. Li, M. Peng, H. Guo, R. Sun, J. Li, Y. Hong, X. Liu, G. Xu, Breast cancer susceptibility protein 1 (BRCA1) rescues neurons from cerebral ischemia/reperfusion injury through NRF2-mediated antioxidant pathway. Redox Biol. 18, 158–172 (2018)
J.R. Becker, G. Clifford, C. Bonnet, A. Groth, M.D. Wilson, J.R. Chapman, BARD1 reads H2A lysine 15 ubiquitination to direct homologous recombination. Nature. 596, 433–437 (2021)
D.T. Bau, Y.C. Mau, C.Y. Shen, The role of BRCA1 in non-homologous end-joining. Cancer Lett. 240, 1–8 (2006)
W. Zhao, J.B. Steinfeld, F. Liang, X. Chen, D.G. Maranon, C. Jian Ma, Y. Kwon, T. Rao, W. Wang, C. Sheng, X. Song, Y. Deng, J. Jimenez-Sainz, L. Lu, R.B. Jensen, Y. Xiong, G.M. Kupfer, C. Wiese, Greene,P. Sung, BRCA1-BARD1 promotes RAD51-mediated homologous DNA pairing. Nature. 550, 360–365 (2017)
D.K. Alves-Fernandes, M.G. Jasiulionis, The role of SIRT1 on DNA damage response and epigenetic alterations in Cancer. Int. J. Mol. Sci. 20, (2019)
D.S. Yoon, Y. Choi, J.W. Lee, Cellular localization of NRF2 determines the self-renewal and osteogenic differentiation potential of human MSCs via the P53-SIRT1 axis. Cell Death Dis. 7, e2093 (2016)
Y. Kawai, L. Garduno, M. Theodore, J. Yang, I.J. Arinze, Acetylation-deacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization. J. Biol. Chem. 286, 7629–7640 (2011)
L. Wang, M.E.A. Howell, A. Sparks-Wallace, C. Hawkins, C.A. Nicksic, C. Kohne, K.H. Hall, J.P. Moorman, Z.Q. Yao, S. Ning, p62-mediated selective autophagy endows virus-transformed cells with insusceptibility to DNA damage under oxidative stress. PLoS. Pathog. 15, e1007541 (2019)
Y. Wang, N. Zhang, L. Zhang, R. Li, W. Fu, K. Ma, X. Li, L. Wang, J. Wang, H. Zhang, W. Gu, W.G. Zhu, Y. Zhao, Autophagy regulates chromatin ubiquitination in DNA damage response through elimination of SQSTM1/p62. Mol. Cell. 63, 34–48 (2016)
P. Schwertman, S. Bekker-Jensen, N. Mailand, Regulation of DNA double-strand break repair by ubiquitin and ubiquitin-like modifiers. Nat. Rev. Mol. Cell. Biol. 17, 379–394 (2016)
L. Zhao, C. Bao, Y. Shang, X. He, C. Ma, X. Lei, D. Mi, Y. Sun, The Determinant of DNA Repair Pathway Choices in Ionising Radiation-Induced DNA Double-Strand Breaks. Biomed. Res. Int. 2020, 4834965 (2020)
F. Zhang, Z. Gong, Regulation of DNA double-strand break repair pathway choice: a new focus on 53BP1. J. Zhejiang Univ. Sci. B 22, 38–46 (2021)
W.C.M. Dempke, M. Reck, KEAP1/NRF2 (NFE2L2) mutations in NSCLC - fuel for a superresistant phenotype? Lung Cancer. 159, 10–17 (2021)
H. Xu, J. Wu, L. Zhang, Y. Li, L. Gao, Y. Cheng, The measurement of NRF2 and TP53 in blood expects radiotherapeutic sensitivity in patients with esophageal cancer. Mol. Cell. Probes. 66, 101860 (2022)
J. Zhang, Q. Jiao, L. Kong, J. Yu, A. Fang, M. Li, J. Yu, Nrf2 and Keap1 abnormalities in esophageal squamous cell carcinoma and association with the effect of chemoradiotherapy. Thorac. Cancer. 9, 726–735 (2018)
P. Telkoparan-Akillilar, E. Panieri, D. Cevik, S. Suzen, L. Saso, Therapeutic targeting of the NRF2 Signaling Pathway in Cancer. Mol. 26, (2021)
H. Kitamura, H. Motohashi, NRF2 addiction in cancer cells. Cancer Sci. 109, 900–911 (2018)
L. Torrente, G.M. DeNicola, Targeting NRF2 and its downstream processes: Opportunities and Challenges. Annu. Rev. Pharmacol. Toxicol. 62, 279–300 (2022)
A.A. Zimta, D. Cenariu, A. Irimie, L. Magdo, S.M. Nabavi, A.G. Atanasov, I. Berindan-Neagoe, the role of Nrf2 activity in Cancer Development and Progression. Cancers (Basel). 11, (2019)
S. Wu, H. Lu, Y. Bai, Nrf2 in cancers: a double-edged sword. Cancer Med. 8, 2252–2267 (2019)
E. Panieri, L. Saso, Potential Applications of NRF2 Inhibitors in Cancer Therapy. Oxid Med Cell Longev. 2019, 8592348 (2019)
N. Robledinos-Anton, R. Fernandez-Gines, G. Manda, A. Cuadrado, Activators and Inhibitors of NRF2: A Review of Their Potential for Clinical Development. Oxid. Med. Cell Longev. 2019, 9372182 (2019)
M. Sova, L. Saso, Design and development of Nrf2 modulators for cancer chemoprevention and therapy: a review. Drug Des. Devel Ther. 12, 3181–3197 (2018)
L.Y. Li, Y.D. Guan, X.S. Chen, J.M. Yang, Y. Cheng, DNA repair pathways in Cancer Therapy and Resistance. Front. Pharmacol. 11, 629266 (2020)
A. Motegi, M. Masutani, K.I. Yoshioka, T. Bessho, Aberrations in DNA repair pathways in cancer and therapeutic significances. Semin Cancer Biol. 58, 29–46 (2019)
M.K. Kwak, K. Itoh, M. Yamamoto, T.W. Kensler, Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 22, 2883–2892 (2002)
A. Dhenaut, S. Boiteux, J.P. Radicella, Characterization of the hOGG1 promoter and its expression during the cell cycle. Mutat. Res. 461, 109–118 (2000)
A. Jain, T. Lamark, E. Sjottem, K.B. Larsen, J.A. Awuh, A. Overvatn, M. McMahon, J.D. Hayes, T. Johansen, p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 285, 22576–22591 (2010)
Funding
This work was supported by grants from the National Natural Science Foundation of China (32171239 and 82273580), CAMS Innovation Fund for Medical Science (2021-I2M-1-042), CIRP Open Fund of Radiation Protection Laboratories (CIRP-DTRI20220202).
Author information
Authors and Affiliations
Contributions
All authors contributed to the outline and content of the article. The first draft of the manuscript was written by Jiale Li and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethical approval
Not applicable.
Statements and Declarations
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, J., Xu, C. & Liu, Q. Roles of NRF2 in DNA damage repair. Cell Oncol. 46, 1577–1593 (2023). https://doi.org/10.1007/s13402-023-00834-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13402-023-00834-5