Cited by 2,882DNA Repair MechanismsEffects of Radiation ExposureCRISPR and Genetic Engineering

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The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway

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Lieber, Michael R.·2010·Annual Review of Biochemistry

DOI 10.1146/annurev.biochem.052308.093131PMC PMC3079308

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Abstract

Double-strand DNA breaks are common events in eukaryotic cells, and there are two major pathways for repairing them: homologous recombination (HR) and nonhomologous DNA end joining (NHEJ). The various causes of double-strand breaks (DSBs) result in a diverse chemistry of DNA ends that must be repaired. Across NHEJ evolution, the enzymes of the NHEJ pathway exhibit a remarkable degree of structural tolerance in the range of DNA end substrate configurations upon which they can act. In vertebrate cells, the nuclease, DNA polymerases, and ligase of NHEJ are the most mechanistically flexible and multifunctional enzymes in each of their classes. Unlike repair pathways for more defined lesions, NHEJ repair enzymes act iteratively, act in any order, and can function independently of one another at each of the two DNA ends being joined. NHEJ is critical not only for the repair of pathologic DSBs as in chromosomal translocations, but also for the repair of physiologic DSBs created during variable (diversity) joining [V(D)J] recombination and class switch recombination (CSR). Therefore, patients lacking normal NHEJ are not only sensitive to ionizing radiation (IR), but also severely immunodeficient.

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Hydroperoxide metabolism in mammalian organs.
Chance, B., Sies, H., & Boveris, A. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.3.527 · Cited by 5,827
DNA Repair and Mutagenesis
Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (2005) · doi:10.1128/9781555816704 · Cited by 5,683
Mechanism of Eukaryotic Homologous Recombination
Filippo, J. S., Sung, P., & Klein, H. L. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.061306.125255 · Cited by 1,766
Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage
Falck, J., Coates, J., & Jackson, S. P. (2005) · Nature · doi:10.1038/nature03442 · Cited by 1,304
Meiotic Chromosomes: Integrating Structure and Function
Zickler, D., & Kleckner, N. E. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.603 · Cited by 1,256
Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair
Walker, J. R., Corpina, R. A., & Goldberg, J. D. (2001) · Nature · doi:10.1038/35088000 · Cited by 1,216
Structural Determinants of Phosphoinositide 3-Kinase Inhibition by Wortmannin, LY294002, Quercetin, Myricetin, and Staurosporine
Walker, E. H., Pacold, M. E., Perišić, O., Stephens, L., Hawkins, P. T., Wymann, M. P., & Williams, R. L. (2000) · Molecular Cell · doi:10.1016/s1097-2765(05)00089-4 · Cited by 1,211
Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination
Ma, Y., Pannicke, U., Schwarz, K., & Lieber, M. R. (2002) · Cell · doi:10.1016/s0092-8674(02)00671-2 · Cited by 1,166
Self-citation
ATM and DNA-PK Function Redundantly to Phosphorylate H2AX after Exposure to Ionizing Radiation
Stiff, T., O’Driscoll, M., Rief, N., Iwabuchi, K., Löbrich, M., & Jeggo, P. A. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3207 · Cited by 1,050
The Mechanism and Regulation of Chromosomal V(D)J Recombination
Bassing, C. H., Swat, W., & Alt, F. W. (2002) · Cell · doi:10.1016/s0092-8674(02)00675-x · Cited by 1,006

Show all 168 references

Research works printed but not linked: 5

Martin GM, 1985, Isr. J. Med. Sci., 21, 296
Wilson TE, 2009, Wiley Encyclopedia of Chemical Biology, 3, 423
Welzel N, 2001, Cancer Res., 61, 1629
van der Burg M, 2009, J. Clin. Investig., 119, 91
Kornberg A, 1992, DNA Replication

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Kujoth, G. C., Sullivan, T. D., Merkhofer, R. M., Lee, T.-J., Wang, H., Brandhorst, T. T., Wüthrich, M., & Klein, B. S. (2018) · mBio · doi:10.1128/mbio.00412-18 · Cited by 58
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Kroth, P. G., Bones, A. M., Daboussi, F., Ferrante, M. I., Jaubert, M. J., Kolot, M., Nymark, M., Bártulos, C. R., Ritter, A., Russo, M. T., et al. (2018) · Plant Cell Reports · doi:10.1007/s00299-018-2334-1 · Cited by 59
DNA ligase III and DNA ligase IV carry out genetically distinct forms of end joining in human somatic cells
Oh, S., Harvey, A., Zimbric, J., Wang, Y., Nguyen, T., Jackson, P. J., & Hendrickson, E. A. (2014) · DNA Repair · doi:10.1016/j.dnarep.2014.04.015 · Cited by 58
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Singh, P., & Ali, S. A. (2021) · Veterinary Sciences · doi:10.3390/vetsci8070122 · Cited by 64
Anti-apoptotic Protein BCL2 Down-regulates DNA End Joining in Cancer Cells
Tadi, S. K., Kari, V., Choudhary, B., Nambiar, M., Akila, T. S., & Raghavan, S. C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.140350 · Cited by 57
Role for the Mammalian Swi5-Sfr1 Complex in DNA Strand Break Repair through Homologous Recombination
Akamatsu, Y., & Jasin, M. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001160 · Cited by 58
Activation of DNA Damage Response Pathways during Lytic Replication of KSHV
Hollingworth, R., Skalka, G., Stewart, G. S., Hislop, A. D., Blackbourn, D. J., & Grand, R. J. A. (2015) · Viruses · doi:10.3390/v7062752 · Cited by 60
RECQ helicase RECQL4 participates in non-homologous end joining and interacts with the Ku complex
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Gene editing in mouse zygotes using the CRISPR/Cas9 system
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Loc'h, J., & Delarue, M. H. (2018) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2018.03.019 · Cited by 57
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Mehrabi, R., Gohari, A. M., & Kema, G. H. J. (2017) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-080615-095928 · Cited by 55
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The Role of Long Non Coding RNAs in the Repair of DNA Double Strand Breaks.
Dianatpour, A., & Ghafouri‐Fard, S. (2017) · PubMed Central · Cited by 56
Refinement of high-risk endometrial cancer classification using DNA damage response biomarkers: a TransPORTEC initiative
Auguste, A., Genestie, C., de Bruyn, M., Adam, J., Formal, A. L., Drusch, F., Pautier, P., Crosbie, E. J., MacKay, H. J., Kitchener, H. C., et al. (2018) · Modern Pathology · doi:10.1038/s41379-018-0055-1 · Cited by 56
RNA therapeutics: Identification of novel targets leading to drug discovery
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Invasive Insects: Management Methods Explored
McLaughlin, G. M., & Dearden, P. K. (2019) · Journal of Insect Science · doi:10.1093/jisesa/iez085 · Cited by 58
The role of histone H3K36me3 writers, readers and erasers in maintaining genome stability
Sharda, A., & Humphrey, T. C. (2022) · DNA repair · doi:10.1016/j.dnarep.2022.103407 · Cited by 63
Sumoylation regulates EXO1 stability and processing of DNA damage
Bologna, S., Altmannová, V., Valtorta, E., Koenig, C., Liberali, P., Gentili, C., Anrather, D., Ammerer, G., Pelkmans, L., Krejčí, L., et al. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1060381 · Cited by 55
Origin of Immunoglobulin Isotype Switching
Zhu, C. Y., Lee, V., Finn, A., Senger, K., Zarrin, A. A., Pasquier, L. D., & Hsu, E. (2012) · Current Biology · doi:10.1016/j.cub.2012.03.060 · Cited by 55
Amplicon rearrangements during the extrachromosomal and intrachromosomal amplification process in a glioma
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Self-citation
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Sebastian, R., & Raghavan, S. C. (2016) · Carcinogenesis · doi:10.1093/carcin/bgw081 · Cited by 55
Biasing genome-editing events toward precise length deletions with an RNA-guided TevCas9 dual nuclease
Wolfs, J. M., Hamilton, T. A., Lant, J. T., Laforet, M., Zhang, J., Salemi, L. M., Gloor, G. B., Schild‐Poulter, C., & Edgell, D. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616343114 · Cited by 56
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Yumlu, S., Stumm, J., Bashir, S., Dreyer, A.-K., Lisowski, P., Danner, E. W., & Kühn, R. (2017) · Methods · doi:10.1016/j.ymeth.2017.05.009 · Cited by 60
BRCA2 antagonizes classical and alternative nonhomologous end-joining to prevent gross genomic instability
Han, J., Ruan, C., Huen, M. S. Y., Wang, J., Xie, A., Fu, C. M., Liu, T., & Huang, J. (2017) · Nature Communications · doi:10.1038/s41467-017-01759-y · Cited by 55
Germline and somatic mutations of homologous recombination-associated genes in Japanese ovarian cancer patients
Sugino, K., Tamura, R., Nakaoka, H., Yachida, N., Yamaguchi, M., Mori, Y., Yamawaki, K., Suda, K., Ishiguro, T., Adachi, S., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-54116-y · Cited by 54
GCNA Interacts with Spartan and Topoisomerase II to Regulate Genome Stability
Dokshin, G. A., Davis, G. M., Sawle, A., Eldridge, M., Nicholls, P. K., Gourley, T. E., Romer, K. A., Molesworth, L. W., Tatnell, H. R., Ozturk, A. R., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.11.006 · Cited by 55
Molecular Spectroscopic Markers of DNA Damage
Sofińska, K., Wilkosz, N., Szymoński, M., & Lipiec, E. W. (2020) · Molecules · doi:10.3390/molecules25030561 · Cited by 59
Immunofluorescence-Based Methods to Monitor DNA End Resection
Mukherjee, B., Tomimatsu, N., & Burma, S. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2522-3_5 · Cited by 55
Telomere fusions in early human breast carcinoma
Tanaka, H., Abe, S., Huda, N., Tu, L., Beam, M. J., Grimes, B., & Gilley, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120062109 · Cited by 52
Lamin B1 sequesters 53BP1 to control its recruitment to DNA damage
Etourneaud, L., Moussa, A., Rass, E., Genet, D., Willaume, S., Chabance-Okumura, C., Wanschoor, P., Picotto, J., Thézé, B., Dépagne, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abb3799 · Cited by 54
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Wu, F., Li, N., Xiao, Y., Palanki, R., Yamagata, H. M., Mitchell, M. J., & Han, X. (2025) · Small Methods · doi:10.1002/smtd.202401632 · Cited by 64
Dental methacrylates may exert genotoxic effects via the oxidative induction of DNA double strand breaks and the inhibition of their repair
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Genetic polymorphisms of DNA double-strand break repair pathway genes and glioma susceptibility
Zhao, P., Zou, P., Zhao, L., Yan, W., Kang, C., Jiang, T., & You, Y. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-234 · Cited by 52
Ku-Mediated Coupling of DNA Cleavage and Repair during Programmed Genome Rearrangements in the Ciliate Paramecium tetraurelia
Marmignon, A., Bischerour, J., Silve, A., Fojcik, C., Dubois, E., Arnaiz, O., Kapusta, A., Malinsky, S., & Bétermier, M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004552 · Cited by 54
Heritability of targeted gene modifications induced by plant-optimized CRISPR systems
Mao, Y., Botella, J. R., & Zhu, J. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2380-1 · Cited by 55
Autocyclized and oxidized forms of SCR 7 induce cancer cell death by inhibiting nonhomologous DNA end joining in a Ligase IV dependent manner
Vartak, S. V., Swarup, H. A., Gopalakrishnan, V., Gopinatha, V. K., Ropars, V., Nambiar, M., John, F., Kothanahally, S. K. S., Kumari, R., Kumari, N., et al. (2018) · FEBS Journal · doi:10.1111/febs.14661 · Cited by 53
Endogenous DNA Double-Strand Breaks during DNA Transactions: Emerging Insights and Methods for Genome-Wide Profiling
Bouwman, B. A. M., & Crosetto, N. (2018) · Genes · doi:10.3390/genes9120632 · Cited by 65
The recent advances in non-homologous end-joining through the lens of lymphocyte development
Wang, X. S., Lee, B. J., & Zha, S. (2020) · DNA repair · doi:10.1016/j.dnarep.2020.102874 · Cited by 54
The X-linked trichothiodystrophy-causing gene RNF113A links the spliceosome to cell survival upon DNA damage
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Authors: Lieber, M. R.
Affiliations: University of Southern California (US)
Corresponding author: Lieber, Michael R.
ORCID: Lieber, Michael R.
Venue: Annual Review of Biochemistry
Publisher: Annual Reviews
Published: 2010-06-07
Volume: 79
Issue: 1
Pages: 181-211
ISSN: 0066-4154 (ISSN-L)
1545-4509
DOI: 10.1146/annurev.biochem.052308.093131
PMC: PMC3079308
OpenAlex: W2164995160
Cited by: 2,882
References: 168
Citations by year: 2026: 103 · 2025: 144 · 2024: 176 · 2023: 148 · 2022: 199 · 2021: 238 · 2020: 209 · 2019: 187 · 2018: 201 · 2017: 215 · 2016: 212 · 2015: 183 · 2014: 199 · 2013: 168 · 2012: 148
FWCI: 13.03
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Annual Review of Biochemistry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA100504)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Keywords: DNA double-strand break repair, non-homologous end joining, homologous recombination, DNA ligase IV, DNA polymerase IV, chromosomal translocation, V(D)J recombination, class switch recombination, immunodeficiency, radiosensitivity
MeSH terms: Animals, Deoxyribonucleases, DNA-Directed DNA Polymerase, DNA Repair, Humans, DNA Ligases, DNA Breaks, Double-Stranded

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The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway

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