Repair of DNA Double-Strand Breaks by the Nonhomologous End Joining Pathway

Stinson, Benjamin M.; Loparo, Joseph J.

doi:10.1146/annurev-biochem-080320-110356

Cited by 229DNA Repair MechanismsEffects of Radiation ExposureCRISPR and Genetic Engineering

The DOI matches its Crossref record; 173 of the 173 references it cites were found in a registry or an index.

Repair of DNA Double-Strand Breaks by the Nonhomologous End Joining Pathway

Open access

Stinson, Benjamin M., Loparo, Joseph J.·2021·Annual Review of Biochemistry

DOI 10.1146/annurev-biochem-080320-110356PMC PMC8899865

Open this paper in CoChat — free account Open PDF

Abstract

DNA double-strand breaks pose a serious threat to genome stability. In vertebrates, these breaks are predominantly repaired by nonhomologous end joining (NHEJ), which pairs DNA ends in a multiprotein synaptic complex to promote their direct ligation. NHEJ is a highly versatile pathway that uses an array of processing enzymes to modify damaged DNA ends and enable their ligation. The mechanisms of end synapsis and end processing have important implications for genome stability. Rapid and stable synapsis is necessary to limit chromosome translocations that result from the mispairing of DNA ends. Furthermore, end processing must be tightly regulated to minimize mutations at the break site. Here, we review our current mechanistic understanding of vertebrate NHEJ, with a particular focus on end synapsis and processing.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1146/annurev-biochem-080320-110356

Cites

173 of 173 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

NHEJ repairs double-strand breaks and infrequently results in insertions or deletions that can disrupt gene function.
“NHEJ operates by recognizing DSBs, processing the DNA ends, and ligating them, infrequently resulting in insertions or deletions (indels) that can disrupt gene function (Stinson & Loparo, 2021; Takata et al., 1998).”
From CRISPR/Cas9 Ribonucleoprotein Nucleofection for Genome Editing in Primary Human Keratinocytes: Knockouts, Deletions, and Homology‐Directed Repair Mutagenesis (2024) · cites this paper as Stinson & Loparo, 2021

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway
Lieber, M. R. (2010) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.052308.093131 · Cited by 2,882
DNA Topoisomerases: Structure, Function, and Mechanism
Champoux, J. J. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.369 · Cited by 2,804
Massive genomic rearrangement acquired in a single catastrophic event during cancer development
Stephens, P. J., Greenman, C. D., Fu, B., Yang, F., Bignell, G. R., Mudie, L. J., Pleasance, E. D., Lau, K. W., Beare, D., Stebbings, L. A., et al. (2011) · Cell · doi:10.1016/j.cell.2010.11.055 · Cited by 2,414
Double-Strand Break End Resection and Repair Pathway Choice
Symington, L. S., & Gautier, J. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132435 · Cited by 1,556
DNA double-strand break repair-pathway choice in somatic mammalian cells
Scully, R., Panday, A., Elango, R., & Willis, N. A. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0152-0 · Cited by 1,532
Repair Pathway Choices and Consequences at the Double-Strand Break
Ceccaldi, R., Rondinelli, B., & D’Andrea, A. D. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.07.009 · Cited by 1,499
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 1,301
Homologous recombination and non‐homologous end‐joining pathways of DNA double‐strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells
Takata, M., Sasaki, M. S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi‐Iwai, Y., Shinohara, A., & Takeda, S. (1998) · The EMBO Journal · doi:10.1093/emboj/17.18.5497 · Cited by 1,229
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
Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells
Chu, V. T., Weber, T., Wefers, B., Wurst, W., Sander, S., Rajewsky, K., & Kühn, R. (2015) · Nature Biotechnology · doi:10.1038/nbt.3198 · Cited by 1,210
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
Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining
Maruyama, T., Dougan, S. K., Truttmann, M. C., Bilate, A. M., Ingram, J. R., & Ploegh, H. L. (2015) · Nature Biotechnology · doi:10.1038/nbt.3190 · Cited by 1,137
Single-strand break repair and genetic disease
Caldecott, K. W. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2380 · Cited by 1,097
Repair of Strand Breaks by Homologous RecombinationPreprint
Jasin, M., & Rothstein, R. J. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012740 · Cited by 929
A Pathway of Double-Strand Break Rejoining Dependent upon ATM, Artemis, and Proteins Locating to γ-H2AX Foci
Riballo, E., Kühne, M., Rief, N., Doherty, A., Smith, G. C. M., Recio, M.-J., Reis, C., Dahm, K., Fricke, A., Krempler, A., et al. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.10.029 · Cited by 837
Shelterin-Mediated Telomere Protection
de Lange, T. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-032918-021921 · Cited by 816
XLF Interacts with the XRCC4-DNA Ligase IV Complex to Promote DNA Nonhomologous End-Joining
Ahnesorg, P., Smith, P., & Jackson, S. P. (2006) · Cell · doi:10.1016/j.cell.2005.12.031 · Cited by 794
Cernunnos, a Novel Nonhomologous End-Joining Factor, Is Mutated in Human Immunodeficiency with Microcephaly
Buck, D., Malivert, L., de Chasseval, R., Barraud, A., Fondanèche, M.-C., Sanal, O., Plebani, A., Stéphan, J.-L., Hufnagel, M., le Deist, F., et al. (2006) · Cell · doi:10.1016/j.cell.2005.12.030 · Cited by 722
Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer
Vilenchik, M. M., & Knudson, A. G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2135498100 · Cited by 717
Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells
Grawunder, U., Wilm, M. S., Wu, X., Kulesza, P., Wilson, T. E., Mann, M., & Lieber, M. R. (1997) · Nature · doi:10.1038/41358 · Cited by 694
A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis
Gao, Y., Sun, Y., Frank, K. M., Dikkes, P., Fujiwara, Y., Seidl, K. J., Sekiguchi, J. M., Rathbun, G. A., Swat, W., Wang, J., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81714-6 · Cited by 688
Class-switch recombination: interplay of transcription, DNA deamination and DNA repair
Chaudhuri, J., & Alt, F. W. (2004) · Nature reviews. Immunology · doi:10.1038/nri1395 · Cited by 657
Microhomology-Mediated End Joining: A Back-up Survival Mechanism or Dedicated Pathway?
Sfeir, A., & Symington, L. S. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.08.006 · Cited by 636
V(D)J Recombination: Mechanisms of Initiation
Schatz, D. G., & Swanson, P. C. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132552 · Cited by 634
DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion
Celli, G. B., & de Lange, T. (2005) · Nature Cell Biology · doi:10.1038/ncb1275 · Cited by 623
IgH class switching and translocations use a robust non-classical end-joining pathway
Yan, C. T., Boboilă, C., Souza, E. K., Franco, S., Hickernell, T. R., Murphy, M., Gumaste, S., Geyer, M. B., Zarrin, A. A., Manis, J. P., et al. (2007) · Nature · doi:10.1038/nature06020 · Cited by 598
Late embryonic lethality and impaired V (D)J recombination in mice lacking DNA ligase IV
Frank, K. M., Sekiguchi, J., Seidl, K. J., Swat, W., Rathbun, G. A., Cheng, H.-L., Davidson, L., Kangaloo, L., & Alt, F. W. (1998) · Nature · doi:10.1038/24172 · Cited by 594
Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks
Kruhlak, M. J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Müller, W. G., McNally, J. G., Bazett-Jones, D. P., & Nussenzweig, A. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200510015 · Cited by 518
Regulation of Single-Strand Annealing and its Role in Genome Maintenance
Bhargava, R., Onyango, D. O., & Stark, J. M. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.06.007 · Cited by 512
Positional stability of single double-strand breaks in mammalian cells
Soutoglou, E., Dorn, J. F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., Danuser, G., & Misteli, T. (2007) · Nature Cell Biology · doi:10.1038/ncb1591 · Cited by 509
Lack of N Regions in Antigen Receptor Variable Region Genes of TdT-Deficient Lymphocytes
Komori, T., Okada, A., Stewart, V., & Alt, F. W. (1993) · Science · doi:10.1126/science.8356451 · Cited by 483
Mechanisms of Programmed DNA Lesions and Genomic Instability in the Immune System
Alt, F. W., Zhang, Y., Meng, F., Guo, C., & Schwer, B. (2013) · Cell · doi:10.1016/j.cell.2013.01.007 · Cited by 477
Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction.
Roth, D. B., & Wilson, J. H. (1986) · Molecular and Cellular Biology · doi:10.1128/mcb.6.12.4295 · Cited by 461
The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination
Li, Z., Otevrel, T., Gao, Y., Cheng, H.-L., Seed, B., Stamato, T. D., Taccioli, G. E., & Alt, F. W. (1995) · Cell · doi:10.1016/0092-8674(95)90135-3 · Cited by 458
Preclinical Evaluation of a Potent Novel DNA-Dependent Protein Kinase Inhibitor NU7441
Zhao, Y., Thomas, H. D., Batey, M. A., Cowell, I. G., Richardson, C. J., Griffin, R. J., Calvert, H., Newell, D. R., Smith, G. C. M., & Curtin, N. J. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4275 · Cited by 447
Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice
Barnes, D. E., Stamp, G., Rosewell, I. R., Denzel, A., & Lindahl, T. L. (1998) · Current Biology · doi:10.1016/s0960-9822(98)00021-9 · Cited by 438
Quantitative Live Cell Imaging Reveals a Gradual Shift between DNA Repair Mechanisms and a Maximal Use of HR in Mid S Phase
Karanam, K., Kafri, R., Loewer, A., & Lahav, G. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.052 · Cited by 435
Is Non-Homologous End-Joining Really an Inherently Error-Prone Process?
Bétermier, M., Bertrand, P., & López, B. S. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004086 · Cited by 420
A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage
Cortés‐Ledesma, F., El‐Khamisy, S. F., Zuma, M. C., Osborn, K., & Caldecott, K. W. (2009) · Nature · doi:10.1038/nature08444 · Cited by 418
Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks
Uematsu, N., Weterings, E., Yano, K., Morotomi‐Yano, K., Jakob, B., Taucher-Scholz, G., Mari, P., van Gent, D. C., Chen, B. P. C., & Chen, D. J. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200608077 · Cited by 414
A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases.
Yang, S., Burgin, A. B., Huizenga, B. N., Robertson, C. A., Yao, K. C., & Nash, H. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11534 · Cited by 413
Ku Recruits the XRCC4-Ligase IV Complex to DNA Ends
McElhinny, S. A. N., McCarville, J., Snowden, C. M., & Ramsden, D. A. (2020) · PubMed Central · doi:10.17615/5hds-gb46 · Cited by 402
The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates
Ahel, I., Rass, U., El‐Khamisy, S. F., Katyal, S., Clements, P. M., McKinnon, P. J., Caldecott, K. W., & West, S. C. (2006) · Nature · doi:10.1038/nature05164 · Cited by 383
A Biochemically Defined System for Mammalian Nonhomologous DNA End Joining
Ma, Y., Lu, H., Tippin, B. L., Goodman, M. F., Shimazaki, N., Koiwai, O., Hsieh, C., Schwarz, K., & Lieber, M. R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.11.017 · Cited by 377
End-joining, translocations and cancer
Bunting, S. F., & Nussenzweig, A. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3537 · Cited by 372
Conversion of Topoisomerase I Cleavage Complexes on the Leading Strand of Ribosomal DNA into 5′-Phosphorylated DNA Double-Strand Breaks by Replication Runoff
Strumberg, D., Pilon, A. A., Smith, M. W., Hickey, R. J., Malkas, L. H., & Pommier, Y. G. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.3977-3987.2000 · Cited by 367
Synapsis of DNA ends by DNA‐dependent protein kinase
DeFazio, L. G., Stansel, R. M., Griffith, J. D., & Chu, G. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf299 · Cited by 365
PAXX, a paralog of XRCC4 and XLF, interacts with Ku to promote DNA double-strand break repair
Ochi, T., Blackford, A. N., Coates, J., Jhujh, S. S., Mehmood, S., Tamura, N., Travers, J., Wu, Q., Draviam, V. M., Robinson, C. V., et al. (2015) · Science · doi:10.1126/science.1261971 · Cited by 357
Eukaryotic DNA Ligases: Structural and Functional Insights
Ellenberger, T., & Tomkinson, A. E. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.061306.123941 · Cited by 356
Chromosomal Translocations in Human Cells Are Generated by Canonical Nonhomologous End-Joining
Ghezraoui, H., Piganeau, M., Renouf, B., Renaud, J.-B., Sallmyr, A., Ruis, B., Oh, S., Tomkinson, A. E., Hendrickson, E. A., Giovannangeli, C., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.002 · Cited by 351
AZD7648 is a potent and selective DNA-PK inhibitor that enhances radiation, chemotherapy and olaparib activity
Fok, J. H. L., Ramos‐Montoya, A., Vázquez–Chantada, M., Wijnhoven, P. W. G., Follia, V., James, N. H., Farrington, P. M., Karmokar, A., Willis, S. E., Cairns, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12836-9 · Cited by 347
Long noncoding RNA LINP1 regulates repair of DNA double-strand breaks in triple-negative breast cancer
Zhang, Y., He, Q., Hu, Z., Feng, Y., Fan, L., Tang, Z., Yuan, J., Shan, W., Li, C., Hu, Z., et al. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3211 · Cited by 340
IgH Chain Class Switch Recombination: Mechanism and Regulation
Stavnezer, J., & Schrader, C. E. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401849 · Cited by 339
A Gradient of Template Dependence Defines Distinct Biological Roles for Family X Polymerases in Nonhomologous End Joining
McElhinny, S. A. N., Havener, J. M., García–Díaz, M., Juárez, R., Bębenek, K., Kee, B. L., Blanco, L., Kunkel, T. A., & Ramsden, D. A. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.012 · Cited by 327
Autophosphorylation of the Catalytic Subunit of the DNA-Dependent Protein Kinase Is Required for Efficient End Processing during DNA Double-Strand Break Repair
Ding, Q., Reddy, Y. V. R., Wang, W., Woods, T. L., Douglas, P., Ramsden, D. A., Lees‐Miller, S. P., & Meek, K. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.16.5836-5848.2003 · Cited by 324
Ku complex interacts with and stimulates the Werner proteinPreprint
Cooper, M. P., Machwe, A., Orren, D. K., Brosh, R. M., Ramsden, D. A., & Bohr, V. A. (2000) · Genes & Development · doi:10.1101/gad.14.8.907 · Cited by 320
Regulation of DNA repair pathway choice in S and G2 phases by the NHEJ inhibitor CYREN
Arnoult, N., Correia, A., Ma, J., Merlo, A., Garcia-Gomez, S., Maric, M., Tognetti, M., Benner, C. W., Boulton, S. J., Saghatelian, A., et al. (2017) · Nature · doi:10.1038/nature24023 · Cited by 299
DNA end-joining catalyzed by human cell-free extracts
Baumann, P., & West, S. C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14066 · Cited by 295
The DNA-dependent Protein Kinase Is Inactivated by Autophosphorylation of the Catalytic Subunit
Chan, D. W., & Lees‐Miller, S. P. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.15.8936 · Cited by 291
Chapter 2 DNA-PK
Meek, K., Dang, V. D., & Lees‐Miller, S. P. (2008) · Advances in immunology · doi:10.1016/s0065-2776(08)00602-0 · Cited by 289
The DNA-dependent protein kinase: A multifunctional protein kinase with roles in DNA double strand break repair and mitosis
Jette, N., & Lees‐Miller, S. P. (2014) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2014.12.003 · Cited by 281
Autophosphorylation of DNA-Dependent Protein Kinase Regulates DNA End Processing and May Also Alter Double-Strand Break Repair Pathway Choice
Cui, X., Yu, Y., Gupta, S., Cho, Y., Lees‐Miller, S. P., & Meek, K. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.24.10842-10852.2005 · Cited by 277
Activation of the ATR kinase by the RPA-binding protein ETAA1
Haahr, P., Hoffmann, S., Tollenaere, M. A. X., Ho, T., Toledo, L. I., Mann, M., Bekker‐Jensen, S., Räschle, M., & Mailand, N. (2016) · Nature Cell Biology · doi:10.1038/ncb3422 · Cited by 272
Three-Dimensional Structure of the Human DNA-PKcs/Ku70/Ku80 Complex Assembled on DNA and Its Implications for DNA DSB Repair
Spagnolo, L., Rivera-Calzada, Á., Pearl, L. H., & Llorca, Ó. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.04.013 · Cited by 270
Pharmacological inhibition of DNA-PK stimulates Cas9-mediated genome editing
Robert, F., Barbeau, M., Ethier, S. D., Dostie, J., & Pelletier, J. (2015) · Genome Medicine · doi:10.1186/s13073-015-0215-6 · Cited by 268
The AID enzyme induces class switch recombination in fibroblasts
Okazaki, I., Kinoshita, K., Muramatsu, M., Yoshikawa, K., & Honjo, T. (2002) · Nature · doi:10.1038/nature727 · Cited by 260
Ku Regulates the Non-Homologous End Joining Pathway Choice of DNA Double-Strand Break Repair in Human Somatic Cells
Fattah, F. J., Lee, E. H., Weisensel, N. A., Wang, Y., Lichter, N., & Hendrickson, E. A. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000855 · Cited by 244
Mapping of protein-protein interactions within the DNA-dependent protein kinase complex
Gell, D. A., & Jackson, S. P. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3494 · Cited by 240
Two-Stage Synapsis of DNA Ends during Non-homologous End Joining
Graham, T. G. W., Walter, J. C., & Loparo, J. J. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.010 · Cited by 239
Self-citation
Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV
Koch, C. A., Agyei, R., Galicia, S., Metalnikov, P. S., O’Donnell, E., Starostine, A., Weinfeld, M., & Durocher, D. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600375 · Cited by 237
The E3 ligase RNF8 regulates KU80 removal and NHEJ repair
Feng, L., & Chen, J. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2211 · Cited by 236
DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining
Feldmann, E., Schmiemann, V., Goedecke, W., Reichenberger, S., & Pfeiffer, P. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.13.2585 · Cited by 235
Differential Phosphorylation of DNA-PKcs Regulates the Interplay between End-Processing and End-Ligation during Nonhomologous End-Joining
Jiang, W., Crowe, J. L., Liu, X., Nakajima, S., Wang, Y., Li, C., Lee, B. J., Dubois, R. L., Liu, C., Yu, X., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.02.024 · Cited by 229
Geometry of a complex formed by double strand break repair proteins at a single DNA end: recruitment of DNA-PKcs induces inward translocation of Ku protein
Yoo, S. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.24.4679 · Cited by 228
Human Tdp1 Cleaves a Broad Spectrum of Substrates, Including Phosphoamide Linkages
Interthal, H., Chen, H. J., & Champoux, J. J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508898200 · Cited by 227
Implication of DNA Polymerase λ in Alignment-based Gap Filling for Nonhomologous DNA End Joining in Human Nuclear Extracts
Lee, J. W., Blanco, L., Zhou, T., García–Díaz, M., Bębenek, K., Kunkel, T. A., Wang, Z., & Povirk, L. F. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307913200 · Cited by 212
The ataxia–oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4
Clements, P. M., Breslin, C., Deeks, E. D., Byrd, P. J., Ju, L., Bieganowski, P., Brenner, C., Moreira, M.-C., Taylor, A. M. R., & Caldecott, K. W. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.06.017 · Cited by 203
Conversion of Phosphoglycolate to Phosphate Termini on 3′ Overhangs of DNA Double Strand Breaks by the Human Tyrosyl-DNA Phosphodiesterase hTdp1
Inamdar, K. V., Pouliot, J. J., Zhou, T., Lees‐Miller, S. P., Rasouli‐Nia, A., & Povirk, L. F. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204688200 · Cited by 200
Nonoverlapping Functions of DNA Polymerases Mu, Lambda, and Terminal Deoxynucleotidyltransferase during Immunoglobulin V(D)J Recombination In Vivo
Bertocci, B., Smet, A. D., Weill, J., & Reynaud, C. (2006) · Immunity · doi:10.1016/j.immuni.2006.04.013 · Cited by 197
The clinical impact of deficiency in DNA non-homologous end-joining
Woodbine, L. J., Gennery, A. R., & Jeggo, P. A. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.02.011 · Cited by 196
Ku is a 5′-dRP/AP lyase that excises nucleotide damage near broken ends
Roberts, S. A., Strande, N. T., Burkhalter, M. D., Strom, C. N., Havener, J. M., Hasty, P., & Ramsden, D. A. (2010) · Nature · doi:10.1038/nature08926 · Cited by 196
ATM orchestrates the DNA-damage response to counter toxic non-homologous end-joining at broken replication forks
Balmus, G., Pilger, D., Coates, J., Demir, M., Sczaniecka-Clift, M., Barros, A. C., Woods, M., Fu, B., Yang, F., Chen, E. D., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-07729-2 · Cited by 195
Cernunnos/XLF promotes the ligation of mismatched and noncohesive DNA ends
Tsai, C. J., Kim, S. A., & Chu, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702620104 · Cited by 194
The X family portrait: Structural insights into biological functions of X family polymerases
Moon, A. F., García–Díaz, M., Batra, V. K., Beard, W. A., Bębenek, K., Kunkel, T. A., Wilson, S. H., & Pedersen, L. C. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.05.009 · Cited by 193
trans Autophosphorylation at DNA-Dependent Protein Kinase's Two Major Autophosphorylation Site Clusters Facilitates End Processing but Not End Joining
Meek, K., Douglas, P., Cui, X., Ding, Q., & Lees‐Miller, S. P. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02366-06 · Cited by 193
The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps
Ma, Y., Schwarz, K., & Lieber, M. R. (2005) · DNA repair · doi:10.1016/j.dnarep.2005.04.013 · Cited by 191
DNA-PK as an Emerging Therapeutic Target in Cancer
Mohiuddin, I. S., & Kang, M. H. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00635 · Cited by 188
Interactome analysis identifies a new paralogue of XRCC4 in non-homologous end joining DNA repair pathway
Xing, M., Yang, M., Huo, W., Feng, F., Wei, L., Jiang, W., Ning, S., Yan, Z., Li, W., Wang, Q., et al. (2015) · Nature Communications · doi:10.1038/ncomms7233 · Cited by 180
XRCC4 protein interactions with XRCC4-like factor (XLF) create an extended grooved scaffold for DNA ligation and double strand break repair
Hammel, M., Rey, M., Yu, Y., Mani, R. S., Classen, S., Liu, M., Pique, M. E., Fang, S., Mahaney, B. L., Weinfeld, M., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.272641 · Cited by 179
Organization and dynamics of the nonhomologous end-joining machinery during DNA double-strand break repair
Reid, D. A., Keegan, S., Leo‐Macías, A., Watanabe, G., Strande, N. T., Chang, H. H., Oksuz, B. A., Fenyö, D., Lieber, M. R., Ramsden, D. A., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420115112 · Cited by 178
The Role of the Core Non-Homologous End Joining Factors in Carcinogenesis and Cancer
Sishc, B. J., & Davis, A. J. (2017) · Cancers · doi:10.3390/cancers9070081 · Cited by 178
DNA-PKcs structure suggests an allosteric mechanism modulating DNA double-strand break repair
Sibanda, B. L., Chirgadze, D. Y., Ascher, D. B., & Blundell, T. L. (2017) · Science · doi:10.1126/science.aak9654 · Cited by 177
Ku80 removal from DNA through double strand break–induced ubiquitylation
Postow, L., Ghenoiu, C., Woo, E. M., Krutchinsky, A. N., Chait, B. T., & Funabiki, H. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200802146 · Cited by 172
A human XRCC4–XLF complex bridges DNA
Andres, S. N., Vergnes, A., Ristić, D., Wyman, C., Modesti, M., & Junop, M. S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks022 · Cited by 172
Sliding sleeves of XRCC4–XLF bridge DNA and connect fragments of broken DNA
Brouwer, I., Sitters, G., Candelli, A., Heerema, S. J., Heller, I., de Melo, A. J., Zhang, H., Normanno, D., Modesti, M., Peterman, E. J. G., et al. (2016) · Nature · doi:10.1038/nature18643 · Cited by 166
APLF promotes the assembly and activity of non‐homologous end joining protein complexes
Grundy, G. J., Rulten, S. L., Zeng, Z., Arribas-Bosacoma, R., Iles, N., Manley, K., Oliver, A. W., & Caldecott, K. W. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.304 · Cited by 156
Structural and Functional Interaction between the Human DNA Repair Proteins DNA Ligase IV and XRCC4
Wu, P.-Y., Frit, P., Meesala, S., Dauvillier, S., Modesti, M., Andres, S. N., Huang, Y., Sekiguchi, J., Calsou, P., Salles, B., et al. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01895-08 · Cited by 155
The RNF138 E3 ligase displaces Ku to promote DNA end resection and regulate DNA repair pathway choice
Ismail, I. H., Gagné, J., Genois, M., Strickfaden, H., McDonald, D., Xu, Z., Poirier, G. G., Masson, J., & Hendzel, M. J. (2015) · Nature Cell Biology · doi:10.1038/ncb3259 · Cited by 155
Structural characterization of filaments formed by human Xrcc4–Cernunnos/XLF complex involved in nonhomologous DNA end-joining
Ropars, V., Drevet, P., Legrand, P., Baconnais, S., Amram, J., Faure, G., Márquez, J. A., Piétrement, O., Guérois, R., Callebaut, I., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100758108 · Cited by 153
A novel human AP endonuclease with conserved zinc‐finger‐like motifs involved in DNA strand break responses
Kanno, S., Kuzuoka, H., Sasao, S., Hong, Z., Lan, L., Nakajima, S., & Yasui, A. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601663 · Cited by 153
Crystal Structure of Human XLF: A Twist in Nonhomologous DNA End-Joining
Andres, S. N., Modesti, M., Tsai, C. J., Chu, G., & Junop, M. S. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.10.024 · Cited by 148
DNA Repair: The Search for Homology
Haber, J. E. (2018) · BioEssays · doi:10.1002/bies.201700229 · Cited by 147
Interaction of the Ku heterodimer with the DNA ligase IV/Xrcc4 complex and its regulation by DNA-PK
Costantini, S., Woodbine, L. J., Andreoli, L., Jeggo, P. A., & Vindigni, A. (2007) · DNA repair · doi:10.1016/j.dnarep.2006.12.007 · Cited by 141
Charity begins at home: non-coding RNA functions in DNA repair
Chowdhury, D., Choi, Y. E., & Brault, M. E. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3523 · Cited by 140
Immunoglobulin κ Light Chain Gene Rearrangement Is Impaired in Mice Deficient for DNA Polymerase Mu
Bertocci, B., Smet, A. D., Berek, C., Weill, J., & Reynaud, C. (2003) · Immunity · doi:10.1016/s1074-7613(03)00203-6 · Cited by 140
Neddylation Promotes Ubiquitylation and Release of Ku from DNA-Damage Sites
Brown, J. S., Lukashchuk, N., Sczaniecka-Clift, M., Britton, S., le Sage, C., Calsou, P., Beli, P., Galanty, Y., & Jackson, S. P. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.058 · Cited by 138
Non-homologous End Joining Requires That the DNA-PK Complex Undergo an Autophosphorylation-dependent Rearrangement at DNA Ends
Reddy, Y. V. R., Ding, Q., Lees‐Miller, S. P., Meek, K., & Ramsden, D. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406432200 · Cited by 136
Single-stranded DNA ligation and XLF-stimulated incompatible DNA end ligation by the XRCC4-DNA ligase IV complex: influence of terminal DNA sequence
Gu, J., Lu, H., Tsai, A. G., Schwarz, K., & Lieber, M. R. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm579 · Cited by 136
Nonhomologous end joining: A good solution for bad ends
Waters, C. A., Strande, N. T., Wyatt, D. W., Pryor, J. M., & Ramsden, D. A. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.02.008 · Cited by 132
The DNA-Dependent Protein Kinase Catalytic Subunit Is Phosphorylated In Vivo on Threonine 3950, a Highly Conserved Amino Acid in the Protein Kinase Domain
Douglas, P., Cui, X., Block, W. D., Yu, Y., Gupta, S., Ding, Q., Ye, R., MORRICE, N. A., Lees‐Miller, S. P., & Meek, K. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01962-06 · Cited by 127
The role of DNA dependent protein kinase in synapsis of DNA ends
Weterings, E. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg889 · Cited by 125
Processing of DNA for nonhomologous end‐joining by cell‐free extract
Budman, J., & Chu, G. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600563 · Cited by 121
WRN regulates pathway choice between classical and alternative non-homologous end joining
Shamanna, R. A., Lu, H., de Freitas, J. K., Tian, J. Y., Croteau, D. L., & Bohr, V. A. (2016) · Nature Communications · doi:10.1038/ncomms13785 · Cited by 120
The Catalytic Subunit of DNA-Dependent Protein Kinase Regulates Proliferation, Telomere Length, and Genomic Stability in Human Somatic Cells
Ruis, B. L., Fattah, K. R., & Hendrickson, E. A. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00355-08 · Cited by 119
DNA-PKcs Dependence of Artemis Endonucleolytic Activity, Differences between Hairpins and 5′ or 3′ Overhangs
Niewolik, D., Pannicke, U., Lu, H., Ma, Y., Wang, L.-C. V., Kulesza, P., Zandi, E., Lieber, M. R., & Schwarz, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606023200 · Cited by 118
XLF and APLF bind Ku80 at two remote sites to ensure DNA repair by non-homologous end joining
Nemoz, C., Ropars, V., Frit, P., Gontier, A., Drevet, P., Yu, J., Guérois, R., Pitois, A., Comte, A., Delteil, C., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0133-6 · Cited by 118
XRCC4 and XLF form long helical protein filaments suitable for DNA end protection and alignment to facilitate DNA double strand break repair
Mahaney, B. L., Hammel, M., Meek, K., Tainer, J. A., & Lees‐Miller, S. P. (2012) · Biochemistry and Cell Biology · doi:10.1139/bcb-2012-0058 · Cited by 117
Crystal structure of human XLF/Cernunnos reveals unexpected differences from XRCC4 with implications for NHEJ
Li, Y., Chirgadze, D. Y., Bolaños-García, V. M., Sibanda, B. L., Davies, O. R., Ahnesorg, P., Jackson, S. P., & Blundell, T. L. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601942 · Cited by 116
PAXX Is an Accessory c-NHEJ Factor that Associates with Ku70 and Has Overlapping Functions with XLF
Tadi, S. K., Tellier-Lebègue, C., Nemoz, C., Drevet, P., Audebert, S., Roy, S., Meek, K., Charbonnier, J., & Modesti, M. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.026 · Cited by 115
Repair of Double-Strand DNA Breaks by the Human Nonhomologous DNA End Joining Pathway: The Iterative Processing Model
Ma, Y., Lu, H., Schwarz, K., & Lieber, M. R. (2005) · Cell Cycle · doi:10.4161/cc.4.9.1977 · Cited by 112
DNA-PK and ATM phosphorylation sites in XLF/Cernunnos are not required for repair of DNA double strand breaks
YU, Y., Mahaney, B. L., YANO, K., Ye, R., FANG, S., DOUGLAS, P., Chen, D., & Lees‐Miller, S. P. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.06.015 · Cited by 109
A Mechanism to Minimize Errors during Non-homologous End Joining
Stinson, B. M., Moreno, A., Walter, J. C., & Loparo, J. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.11.018 · Cited by 108
Self-citation
Mechanisms of Overlap Formation in Nonhomologous DNA End Joining
Pfeiffer, P., Thode, S., Hancke, J., & Vielmetter, W. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.2.888 · Cited by 106
MOLECULAR ANALYSIS OF V(D)J RECOMBINATION
Gellert, M. F. (1992) · Annual Review of Genetics · doi:10.1146/annurev.ge.26.120192.002233 · Cited by 106
PAXX and XLF DNA repair factors are functionally redundant in joining DNA breaks in a G1-arrested progenitor B-cell line
Kumar, V., Alt, F. W., & Frock, R. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611882113 · Cited by 106
A noncatalytic function of the ligation complex during nonhomologous end joining
Jessica, C., Frit, P., Bombarde, O., Salles, B., Négrel, A., Bernard, S., Jeggo, P. A., Lieber, M. R., Modesti, M., & Calsou, P. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201203128 · Cited by 105
MRI Is a DNA Damage Response Adaptor during Classical Non-homologous End Joining
Hung, P. J., Johnson, B., Chen, B.-R., Byrum, A. K., Bredemeyer, A. L., Yewdell, W. T., Johnson, T. E., Lee, B. J., Deivasigamani, S., Hindi, I., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.018 · Cited by 105
Phosphorylation of Ku dictates DNA double-strand break (DSB) repair pathway choice in S phase
Lee, K. J., Saha, J., Sun, J., Fattah, K. R., Wang, S.-C., Jakob, B., Chi, L., Wang, S., Taucher-Scholz, G., Davis, A. J., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1499 · Cited by 100
DNA polymerase λ can elongate on DNA substrates mimicking non-homologous end joining and interact with XRCC4–ligase IV complex
Fan, W., & Wu, X. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.002 · Cited by 97
C-NHEJ without indels is robust and requires synergistic function of distinct XLF domains
Bhargava, R., Sandhu, M., Muk, S., Lee, G., Vaidehi, N., & Stark, J. M. (2018) · Nature Communications · doi:10.1038/s41467-018-04867-5 · Cited by 97
The essential elements for the noncovalent association of two DNA ends during NHEJ synapsis
Zhao, B., Watanabe, G., Morten, M. J., Reid, D. A., Rothenberg, E., & Lieber, M. R. (2019) · Nature Communications · doi:10.1038/s41467-019-11507-z · Cited by 95
DNA-PKcs has KU-dependent function in rRNA processing and haematopoiesis
Shao, Z., Flynn, R. A., Crowe, J. L., Zhu, Y., Liang, J., Jiang, W., Aryan, F., Aoude, P., Bertozzi, C. R., Estes, V. M., et al. (2020) · Nature · doi:10.1038/s41586-020-2041-2 · Cited by 95
Pathways and functions of the Werner syndrome protein
Lee, J. W., Harrigan, J. A., Opresko, P. L., & Bohr, V. A. (2004) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2004.09.011 · Cited by 93
Dissection of DNA double-strand-break repair using novel single-molecule forceps
Wang, J., Duboc, C., Wu, Q., Ochi, T., Liang, S., Tsutakawa, S. E., Lees‐Miller, S. P., Nadal, M., Tainer, J. A., Blundell, T. L., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0065-1 · Cited by 90
Ribonucleotide incorporation enables repair of chromosome breaks by nonhomologous end joining
Pryor, J. M., Conlin, M. P., Carvajal-Garcia, J., Luedeman, M. E., Luthman, A. J., Small, G. W., & Ramsden, D. A. (2018) · Science · doi:10.1126/science.aat2477 · Cited by 89
Synthetic lethality between PAXX and XLF in mammalian developmentPreprint
Balmus, G., Barros, A. C., Wijnhoven, P. W. G., Lescale, C., Hasse, H. L., Boroviak, K., le Sage, C., Doe, B., Speak, A. O., Galli, A., et al. (2016) · Genes & Development · doi:10.1101/gad.290510.116 · Cited by 87
The Ku-binding motif is a conserved module for recruitment and stimulation of non-homologous end-joining proteins
Grundy, G. J., Rulten, S. L., Arribas-Bosacoma, R., Davidson, K., Kozik, Z., Oliver, A. W., Pearl, L. H., & Caldecott, K. W. (2016) · Nature Communications · doi:10.1038/ncomms11242 · Cited by 84
Werner Protein Cooperates with the XRCC4-DNA Ligase IV Complex in End-Processing
Kusumoto, R., Dawut, L., Marchetti, C., Lee, J. W., Vindigni, A., Ramsden, D. A., & Bohr, V. A. (2008) · Biochemistry · doi:10.1021/bi702325t · Cited by 81
Plugged into the Ku-DNA hub: The NHEJ network
Frit, P., Ropars, V., Modesti, M., Charbonnier, J., & Calsou, P. (2019) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2019.03.001 · Cited by 81
Ku-Dependent Nonhomologous DNA End Joining in Xenopus Egg Extracts
Labhart, P. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.4.2585 · Cited by 80
The fidelity of the ligation step determines how ends are resolved during nonhomologous end joining
Waters, C. A., Strande, N. T., Pryor, J. M., Strom, C. N., Mieczkowski, P., Burkhalter, M. D., Oh, S., Qaqish, B. F., Moore, D. T., Hendrickson, E. A., et al. (2014) · Nature Communications · doi:10.1038/ncomms5286 · Cited by 78
Distribution and roles of X-family DNA polymerases in eukaryotes
Uchiyama, Y., Takeuchi, R., Kodera, H., & Sakaguchi, K. (2008) · Biochimie · doi:10.1016/j.biochi.2008.07.005 · Cited by 75
XRCC4's interaction with XLF is required for coding (but not signal) end joining
Roy, S., Andres, S. N., Vergnes, A., Neal, J. A., Xu, Y., Yu, Y., Lees‐Miller, S. P., Junop, M. S., Modesti, M., & Meek, K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr1315 · Cited by 72
Functional significance of the interaction with Ku in DNA double-strand break recognition of XLF
Yano, K.-I., Morotomi‐Yano, K., Lee, K. J., & Chen, D. J. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.02.020 · Cited by 69
An SCF complex containing Fbxl12 mediates DNA damage-induced Ku80 ubiquitylation
Postow, L., & Funabiki, H. (2013) · Cell Cycle · doi:10.4161/cc.23408 · Cited by 68
XRCC4/XLF Interaction Is Variably Required for DNA Repair and Is Not Required for Ligase IV Stimulation
Roy, S., de Melo, A. J., Xu, Y., Tadi, S. K., Négrel, A., Hendrickson, E. A., Modesti, M., & Meek, K. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01503-14 · Cited by 67
Essential role for polymerase specialization in cellular nonhomologous end joining
Pryor, J. M., Waters, C. A., Aza, A., Asagoshi, K., Strom, C. N., Mieczkowski, P. A., Blanco, L., & Ramsden, D. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505805112 · Cited by 67
Ubiquitylation of Ku80 by RNF126 Promotes Completion of Nonhomologous End Joining-Mediated DNA Repair
Ishida, N., Nakagawa, T., Iemura, S.-I., Yasui, A., Shima, H., Katoh, Y., Nagasawa, Y., Natsume, T., Igarashi, K., & Nakayama, K. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.00347-16 · Cited by 66
DNA Ligase IV Guides End-Processing Choice during Nonhomologous End Joining
Conlin, M. P., Reid, D. A., Small, G. W., Chang, H. H., Watanabe, G., Lieber, M. R., Ramsden, D. A., & Rothenberg, E. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.091 · Cited by 64
A single XLF dimer bridges DNA ends during nonhomologous end joining
Graham, T. G. W., Carney, S. M., Walter, J. C., & Loparo, J. J. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0120-y · Cited by 62
Self-citation
Requirement for XLF/Cernunnos in alignment-based gap filling by DNA polymerases λ and μ for nonhomologous end joining in human whole-cell extracts
Akopiants, K., Zhou, R.-Z., Mohapatra, S., Valerie, K. C., Lees‐Miller, S. P., Lee, K.-J., Chen, D. J., Revy, P., de Villartay, J., & Povirk, L. F. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp283 · Cited by 55
Biochemical Characterization of Metnase’s Endonuclease Activity and Its Role in NHEJ Repair
Beck, B. D., Lee, S.-S., Williamson, E. A., Hromas, R., & Lee, S. (2011) · Biochemistry · doi:10.1021/bi200333k · Cited by 54
Non‐homologous end joining: Common interaction sites and exchange of multiple factors in the DNA repair process
Rulten, S. L., & Grundy, G. J. (2017) · BioEssays · doi:10.1002/bies.201600209 · Cited by 50
Suppressing Ku70/Ku80 expression elevates homology-directed repair efficiency in primary fibroblasts
Li, G., Liu, D., Zhang, X., Quan, R., Zhong, C., Mo, J., Huang, Y., Wang, H., Xiao-fang, R. U. A. N., Xu, Z., et al. (2018) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2018.04.011 · Cited by 50
Structural dynamics in DNA damage signaling and repair
Perry, J. J. P., Cotner‐Gohara, E., Ellenberger, T., & Tainer, J. A. (2010) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2010.03.012 · Cited by 49
Structural Insights into the Role of Domain Flexibility in Human DNA Ligase IV
Ochi, T., Wu, Q., Chirgadze, D. Y., Grossmann, J. G., Bolaños-García, V. M., & Blundell, T. L. (2012) · Structure · doi:10.1016/j.str.2012.04.012 · Cited by 49
Polynucleotide Kinase and Aprataxin-like Forkhead-associated Protein (PALF) Acts as Both a Single-stranded DNA Endonuclease and a Single-Stranded DNA 3′ Exonuclease and Can Participate in DNA End Joining in a Biochemical System
Li, S., Kanno, S.-I., Watanabe, R., Ogiwara, H., Kohno, T., Watanabe, G., Yasui, A., & Lieber, M. R. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.287797 · Cited by 48
Requirement for XRCC4 and DNA ligase IV in alignment-based gap filling for nonhomologous DNA end joining in vitro.
Lee, J. W., Yannone, S. M., Chen, D. J., & Povirk, L. F. (2003) · PubMed · Cited by 47
Structural Basis of DNA Ligase IV-Artemis Interaction in Nonhomologous End-Joining
Ioannes, P. D., Malu, S., Cortés, P., & Aggarwal, A. K. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.11.004 · Cited by 47
Bridging of double-stranded breaks by the nonhomologous end-joining ligation complex is modulated by DNA end chemistry
Reid, D. A., Conlin, M. P., Yin, Y., Chang, H. H., Watanabe, G., Lieber, M. R., Ramsden, D. A., & Rothenberg, E. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1221 · Cited by 46
Mutational phospho-mimicry reveals a regulatory role for the XRCC4 and XLF C-terminal tails in modulating DNA bridging during classical non-homologous end joining
Normanno, D., Négrel, A., de Melo, A. J., Betzi, S., Meek, K., & Modesti, M. (2017) · eLife · doi:10.7554/elife.22900 · Cited by 38
PAXX and its paralogs synergistically direct DNA polymerase λ activity in DNA repair
Craxton, A., Munnur, D., Jukes‐Jones, R., Skalka, G., Langlais, C., Cain, K., & Malewicz, M. (2018) · Nature Communications · doi:10.1038/s41467-018-06127-y · Cited by 36
XLF acts as a flexible connector during non-homologous end joining
Carney, S. M., Moreno, A., Piatt, S. C., Cisneros‐Aguirre, M., Lopezcolorado, F. W., Stark, J. M., & Loparo, J. J. (2020) · eLife · doi:10.7554/elife.61920 · Cited by 32
Self-citation
Repair of chromosomal double-strand breaks by precise ligation in human cells
Lin, W. Y., Wilson, J. H., & Lin, Y. (2013) · DNA repair · doi:10.1016/j.dnarep.2013.04.024 · Cited by 30
TDP1 suppresses mis-joining of radiomimetic DNA double-strand breaks and cooperates with Artemis to promote optimal nonhomologous end joining
Kawale, A. S., Akopiants, K., Valerie, K. C., Ruis, B. L., Hendrickson, E. A., Huang, S.-Y. N., Pommier, Y. G., & Povirk, L. F. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky694 · Cited by 28
The roles of the human SETMAR (Metnase) protein in illegitimate DNA recombination and non-homologous end joining repair
Tellier, M., & Chalmers, R. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.06.006 · Cited by 22
Topoisomerase I and Genome Stability: The Good and the Bad
Cho, J.-E., & Jinks-Robertson, S. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7459-7_2 · Cited by 21
Synthetic lethality between murine DNA repair factors XLF and DNA-PKcs is rescued by inactivation of Ku70
Xing, M., Bjørås, M., Daniel, J. A., Alt, F. W., & Oksenych, V. (2017) · DNA repair · doi:10.1016/j.dnarep.2017.07.008 · Cited by 21
Ligand binding characteristics of the Ku80 von Willebrand domain
Kim, K., Min, J., Kirby, T. W., Gabel, S. A., Pedersen, L. C., & London, R. E. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.102739 · Cited by 19
Resolution of complex ends by Nonhomologous end joining - better to be lucky than good?
Strande, N. T., Waters, C. A., & Ramsden, D. A. (2012) · Genome Integrity · doi:10.1186/2041-9414-3-10 · Cited by 15
Two‐way crosstalk between BER and c‐NHEJ repair pathway is mediated by Pol‐β and Ku70
Wen, X., Ci, S., Li, M., Wang, M., Dianov, G. L., Ma, Z., Li, L., Hua, K. Q., Alagamuthu, K. K., Qing, L., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201900308r · Cited by 14
The human DNA ends proteome uncovers an unexpected entanglement of functional pathways
Berthelot, V., Cardoso, G. M., Hégarat, N., Guillonneau, F., François, J., Giovannangeli, C., Praseuth, D., & Rusconi, F. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw121 · Cited by 11
Druggable binding sites in the multicomponent assemblies that characterise DNA double-strand-break repair through non-homologous end joining
Stavridi, A. K., Appleby, R. E., Liang, S., Blundell, T. L., & Chaplin, A. K. (2020) · Essays in Biochemistry · doi:10.1042/ebc20190092 · Cited by 10

Flagged first, then by citations

Research works printed but not linked: 6

10.1128/MCB.20.9.2996-3003.2000 · DOI
10.1038/emboj.2012.304 · DOI
Lee JW, 2003, Cancer Res, 63, 22
Pfeiffer P, 1994, Mol. Cell. Biol., 14, 888
Roth DB, 1986, Mol. Cell. Biol., 6, 4295
10.1038/nature08926 · DOI

Sorted by citations

CRISPR-based genome editing through the lens of DNA repair
Nambiar, T. S., Baudrier, L., Billon, P., & Ciccia, A. (2022) · Molecular Cell · doi:10.1016/j.molcel.2021.12.026 · Cited by 224
Annual review of PROTAC degraders as anticancer agents in 2022
Wang, X., Qin, Z.-L., Li, N., Jia, M.-Q., Liu, Q.-G., Bai, Y., Song, J., Yuan, S., & Zhang, S. (2024) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2024.116166 · Cited by 107
Gene therapy for CNS disorders: modalities, delivery and translational challenges
Gao, J., Gunasekar, S., Xia, Z. J., Shalin, K., Jiang, C., Chen, H., Lee, D., Lee, S., Pisal, N. D., Luo, J. N., et al. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00829-7 · Cited by 100
Recent advances in CRISPR-Cas9-based genome insertion technologies
Chen, X., Du, J., Yun, S., Xue, C., Yao, Y., & Rao, S. (2024) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2024.102138 · Cited by 71
Combining targeted DNA repair inhibition and immune-oncology approaches for enhanced tumor control
Concannon, K., Morris, B. B., Gay, C. M., & Byers, L. A. (2023) · Molecular Cell · doi:10.1016/j.molcel.2022.12.031 · Cited by 71
Liquid-liquid phase separation in DNA double-strand breaks repair
Wang, Y., Zhao, W.-W., Shi, J., Wan, X., Zheng, J., & Fan, X. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-06267-0 · Cited by 62
Small Molecules Targeting DNA Polymerase Theta (POLθ) as Promising Synthetic Lethal Agents for Precision Cancer Therapy
Pismataro, M. C., Astolfi, A., Barreca, M. L., Pacetti, M., Schenone, S., Bandiera, T., Carbone, A., & Massari, S. (2023) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c02101 · Cited by 60
Polymerase theta-helicase promotes end joining by stripping single-stranded DNA-binding proteins and bridging DNA ends
Schaub, J. M., Soniat, M. M., & Finkelstein, I. J. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac119 · Cited by 58
Meiotic DNA breaks drive multifaceted mutagenesis in the human germ line
Hinch, R., Donnelly, P., & Hinch, A. G. (2023) · Science · doi:10.1126/science.adh2531 · Cited by 55
New Facets of DNA Double Strand Break Repair: Radiation Dose as Key Determinant of HR versus c-NHEJ Engagement
Mladenov, E., Mladenova, V., Stuschke, M., & Iliakis, G. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914956 · Cited by 53
PAXX binding to the NHEJ machinery explains functional redundancy with XLF
Dahan, M. S. E., Stavridi, A. K., Frit, P., Hardwick, S. W., Chirgadze, D. Y., de Oliveira, T. M., Andréani, J., Britton, S., Barboule, N., Bossaert, M., et al. (2023) · Science Advances · doi:10.1126/sciadv.adg2834 · Cited by 43
The dark side of homology-directed repair
Al-Zain, A., & Symington, L. S. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103181 · Cited by 43
Crosstalk between SUMOylation and ubiquitylation controls DNA end resection by maintaining MRE11 homeostasis on chromatin
Zhang, T., Yang, H., Zhou, Z., Bai, Y., Wang, J., & Wang, W. (2022) · Nature Communications · doi:10.1038/s41467-022-32920-x · Cited by 40
Disparate Pathways for Extrachromosomal DNA Biogenesis and Genomic DNA Repair
Rose, J. C., Belk, J. A., Wong, I. T.-L., Luebeck, J., Horn, H. T., Dániel, B., Jones, M. G., Yost, K. E., Hung, K. L., Kolahi, K. S., et al. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-23-1117 · Cited by 38
DNA double-strand break end synapsis by DNA loop extrusion
Yang, J. H., Brandão, H. B., & Hansen, A. S. (2023) · Nature Communications · doi:10.1038/s41467-023-37583-w · Cited by 36
Characterizing and controlling CRISPR repair outcomes in nondividing human cells
Ramadoss, G. N., Namaganda, S. J., Kumar, M. M., Hamilton, J. R., Sharma, R. K., Chow, K. G., Workley, L. A., Macklin, B. L., Sun, M., Ha, A. S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-66058-3 · Cited by 35
Structure and mechanism in non-homologous end joining
Vogt, A., & He, Y. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103547 · Cited by 40
Structural analysis of the basal state of the Artemis:DNA-PKcs complex
Watanabe, G., Lieber, M. R., & Williams, D. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac564 · Cited by 33
Cryo-EM visualization of DNA-PKcs structural intermediates in NHEJ
Chen, S., Vogt, A., Lee, L., Naila, T., McKeown, R., Tomkinson, A. E., Lees‐Miller, S. P., & He, Y. (2023) · Science Advances · doi:10.1126/sciadv.adg2838 · Cited by 32
Histone and Chromatin Dynamics Facilitating DNA repair
Mohan, C., Das, C., & Tyler, J. K. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103183 · Cited by 35
DNA Double-Strand Break Repairs and Their Application in Plant DNA Integration
Shen, H., & Li, Z. (2022) · Genes · doi:10.3390/genes13020322 · Cited by 30
TRIM21-dependent target protein ubiquitination mediates cell-free Trim-Away
Mevissen, T. E. T., Prasad, A. V., & Walter, J. C. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112125 · Cited by 31
Nanomaterials-assisted gene editing and synthetic biology for optimizing the treatment of pulmonary diseases
Lei, L., Pan, W., Shou, X., Shao, Y., Ye, S., Zhang, J., Kolliputi, N., & Shi, L. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-02627-w · Cited by 32
GCN5 mediates DNA-PKcs crotonylation for DNA double-strand break repair and determining cancer radiosensitivity
Han, Y., Zhao, H., Li, G., Jin, J., Guo, H., Tan, J., Sun, X., Li, S., Ran, Q., Bai, C., et al. (2024) · British Journal of Cancer · doi:10.1038/s41416-024-02636-4 · Cited by 28
Targeting the DNA damage response in cancer
Guffanti, F., Chiappa, M., & Damia, G. L. M. (2024) · MedComm · doi:10.1002/mco2.788 · Cited by 30
Conversion of Ku80 K568 crotonylation to SUMOylation facilitates DNA non-homologous end joining and cancer radioresistance
Zhao, H., Gao, S., Han, Y., Xie, D., Xuan, L., Huang, X., Luo, J., Ran, Q., Li, G., Guo, H., et al. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02210-1 · Cited by 28
The Chromatin Landscape around DNA Double-Strand Breaks in Yeast and Its Influence on DNA Repair Pathway Choice
Frigerio, C., Nisio, E. D., Galli, M., Colombo, C. V., Negri, R., & Clerici, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043248 · Cited by 29
Recent Advances in the Development of Non-PIKKs Targeting Small Molecule Inhibitors of DNA Double-Strand Break Repair
Kelm, J. M., Samarbakhsh, A., Pillai, A., VanderVere-Carozza, P. S., Aruri, H., Pandey, D. S., Pawelczak, K. S., Turchi, J. J., & Gavande, N. S. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.850883 · Cited by 27
Function and Evolution of the Loop Extrusion Machinery in Animals
Kabirova, E., Nurislamov, A. R., Shadskiy, A., Smirnov, A. V., Popov, A., Salnikov, P., Баттулин, Н. Р., & Fishman, V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24055017 · Cited by 25
Structural role for DNA Ligase IV in promoting the fidelity of non-homologous end joining
Stinson, B. M., Carney, S. M., Walter, J. C., & Loparo, J. J. (2024) · Nature Communications · doi:10.1038/s41467-024-45553-z · Cited by 24
Self-citation
PARP inhibitors in small cell lung cancer: The underlying mechanisms and clinical implications
Wang, X., Zeng, X., Li, D., Zhu, C., Guo, X., Feng, L., & Yu, Z. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113458 · Cited by 24
Structural and functional insights into the interaction between Ku70/80 and Pol X family polymerases in NHEJ
Frit, P., Amin, H., Zahid, S., Barboule, N., Hall, C., Matharu, G., Hardwick, S. W., Chauvat, J., Britton, S., Chirgadze, D. Y., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59133-2 · Cited by 23
Synthesis and biological evaluation of a tumor-selective degrader of PARP1
Pu, C., Wang, S., Luo, D., Liu, Y., Ma, X., Zhang, H., Yu, S., Lan, S., Huang, Q., Deng, R., et al. (2022) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2022.116908 · Cited by 24
Break‐induced RNA–DNA hybrids (BIRDHs) in homologous recombination: friend or foe?
Gómez‐González, B., & Aguilera, A. (2023) · EMBO Reports · doi:10.15252/embr.202357801 · Cited by 23
Potential therapeutic strategies for osteoarthritis via CRISPR/Cas9 mediated gene editing
Vlashi, R., Zhang, X., Li, H., & Chen, G. (2023) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09860-y · Cited by 24
Single-molecule imaging reveals the kinetics of non-homologous end-joining in living cells
Mikhova, M., Goff, N. J., Janovič, T., Heyza, J. R., Meek, K., & Schmidt, J. C. (2024) · Nature Communications · doi:10.1038/s41467-024-54545-y · Cited by 24
The importance of DNAPKcs for blunt DNA end joining is magnified when XLF is weakened
Cisneros‐Aguirre, M., Lopezcolorado, F. W., Tsai, L. J., Bhargava, R., & Stark, J. M. (2022) · Nature Communications · doi:10.1038/s41467-022-31365-6 · Cited by 21
The Ku complex promotes DNA end-bridging and this function is antagonized by Tel1/ATM kinase
Rinaldi, C., Pizzul, P., Casari, E., Mangiagalli, M., Tisi, R., & Longhese, M. P. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad062 · Cited by 20
Holding it together: DNA end synapsis during non-homologous end joining
Loparo, J. J. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103553 · Cited by 20
Self-citation
The FAcilitates Chromatin Transcription (FACT) complex: Its roles in DNA repair and implications for cancer therapy
Bhakat, K. K., & Ray, S. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103246 · Cited by 24
The tripartite motif-containing 24 is a multifunctional player in human cancer
Yao, Y., Zhou, S., Yue, Y., Fu, K., & Xiao, S. (2024) · Cell & Bioscience · doi:10.1186/s13578-024-01289-3 · Cited by 20
In vivo liver targeted genome editing as therapeutic approach: progresses and challenges
Simoni, C., Barbon, E., Muro, A. F., & Cantore, A. (2024) · Frontiers in Genome Editing · doi:10.3389/fgeed.2024.1458037 · Cited by 19
Dynamic assemblies and coordinated reactions of non-homologous end joining
Liu, L., Li, J., Cisneros‐Aguirre, M., Merkell, A., Stark, J. M., Gellert, M. F., & Yang, W. (2025) · Nature · doi:10.1038/s41586-025-09078-9 · Cited by 18
Multivalent interactions of the disordered regions of XLF and XRCC4 foster robust cellular NHEJ and drive the formation of ligation-boosting condensates in vitro
Vu, D.-D., Bonucci, A., Brenière, M., Cisneros‐Aguirre, M., Pelupessy, P., Wang, Z., Carlier, L., Bouvignies, G., Cortés, P., Aggarwal, A. K., et al. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01339-x · Cited by 18
Broad repression of DNA repair genes in senescent cells identified by integration of transcriptomic data
Frey, Y., Haj, M., Ziv, Y., Elkon, R., & Shiloh, Y. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae1257 · Cited by 18
Defective Homologous Recombination Repair By Up‐Regulating Lnc‐HZ10/Ahr Loop in Human Trophoblast Cells Induced Miscarriage
Chen, W., Mi, C., Zhang, Y., Yang, Y., Huang, W., Xu, Z., Zhao, J., Wang, R., Wang, M., Wan, S., et al. (2024) · Advanced Science · doi:10.1002/advs.202207435 · Cited by 17
New Discoveries on Protein Recruitment and Regulation during the Early Stages of the DNA Damage Response Pathways
Waters, K. L., & Spratt, D. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031676 · Cited by 17
Editing of the ethylene biosynthesis gene in carnation using CRISPR-Cas9 ribonucleoprotein complex
Adedeji, O. S., Naing, A. H., Kang, H., Xu, J., Chung, M. Y., & Kim, C. K. (2024) · Plant Methods · doi:10.1186/s13007-024-01143-0 · Cited by 17
Quercetin exhibits cytotoxicity in cancer cells by inducing two-ended DNA double-strand breaks
Someya, Y., Saito, S., Takeda, S., Adachi, N., & Kurosawa, A. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150977 · Cited by 17
APLF and long non-coding RNA NIHCOLE promote stable DNA synapsis in non-homologous end joining
de Bragança, S., Aicart-Ramos, C., Arribas-Bosacoma, R., Rivera-Calzada, Á., Unfried, J. P., Prats-Mari, L., Marín-Baquero, M., Fortes, P., Llorca, Ó., & Moreno‐Herrero, F. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111917 · Cited by 17
DNA repair pathways in breast cancer: from mechanisms to clinical applications
Tufail, M. (2023) · Breast Cancer Research and Treatment · doi:10.1007/s10549-023-06995-z · Cited by 18
The interplay between driver mutation and oxidative stress in colorectal cancer: from pathogenesis to therapeutics
Huang, Q., Jing, Y., Xiong, L., Li, L., Feng, J., & Cheng, J. G. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06640-x · Cited by 18
New insights into the DNA repair pathway choice with NuA4/TIP60
Lashgari, A., Tchara, P.-E. K., Lambert, J., & Côté, J. (2022) · DNA repair · doi:10.1016/j.dnarep.2022.103315 · Cited by 17
Recent insights into eukaryotic double-strand DNA break repair unveiled by single-molecule methods
de Bragança, S., Dillingham, M. S., & Moreno‐Herrero, F. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.09.004 · Cited by 18
The power and the promise of synthetic lethality for clinical application in cancer treatment
Liu, Q., Yang, Z., Tang, Q.-H., Wang, W.-E., Chu, D.-S., Ji, J.-F., Fan, Q.-Y., Jiang, H., Yang, Q.-X., Zhang, H., et al. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116288 · Cited by 17
Identification of the main barriers to Ku accumulation in chromatin
Bossaert, M., Moreno, A., Peixoto, A., Pillaire, M., Chanut, P., Frit, P., Calsou, P., Loparo, J. J., & Britton, S. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114538 · Cited by 17
Self-citation
CST/Polα/primase-mediated fill-in synthesis at DSBs
Mirman, Z., Cai, S. W., & de Lange, T. (2022) · Cell Cycle · doi:10.1080/15384101.2022.2123886 · Cited by 16
The role of SWI/SNF chromatin remodelers in the repair of DNA double strand breaks and cancer therapy
Sadek, M., Sheth, A., Zimmerman, G., Hays, E., & Vélez-Cruz, R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1071786 · Cited by 18
Kaempferol inhibits non-homologous end joining repair via regulating Ku80 stability in glioma cancer
Chen, M., Zhao, E., Li, M., Xu, M., Hao, S., Gao, Y., Wu, X., Li, X., Yu, Y., Yu, Z., et al. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154876 · Cited by 15
DNA repair deficiency and the immune microenvironment: A pathways perspective
Zhou, Y., & Mouw, K. W. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103594 · Cited by 15
Poly (ADP-ribose) polymerase inhibitor therapy and mechanisms of resistance in epithelial ovarian cancer
Kulkarni, S., Gajjar, K. B., & Madhusudan, S. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1414112 · Cited by 15
Mechanistic Insights From Single-Molecule Studies of Repair of Double Strand Breaks
Kong, M., & Greene, E. C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.745311 · Cited by 17
Long non‑coding RNAs interact with RNA‑binding proteins to regulate genomic instability in cancer cells (Review)
Yang, K., Liang, X., & Wen, K. (2022) · Oncology Reports · doi:10.3892/or.2022.8390 · Cited by 15
Bone Marrow Failure and Immunodeficiency Associated with Human RAD50 Variants
Takagi, M., Hoshino, A., Bousset, K., Röddecke, J., Martin, H. L., Folcut, I., Tomomasa, D., Yang, X., Kobayashi, J., Sakata, N., et al. (2023) · Journal of Clinical Immunology · doi:10.1007/s10875-023-01591-8 · Cited by 14
TDP1 represents a promising therapeutic target for overcoming tumor resistance to chemotherapeutic agents: progress and potential
Zhang, M., Wang, Z., Su, Y. A., Yan, W., Ouyang, Y., Fan, Y., Yu, Y., & Yang, H. C. (2024) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2024.108072 · Cited by 13
Rif2 interaction with Rad50 counteracts Tel1 functions in checkpoint signalling and DNA tethering by releasing Tel1 from MRX binding
Pizzul, P., Casari, E., Rinaldi, C., Gnugnoli, M., Mangiagalli, M., Tisi, R., & Longhese, M. P. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkad1246 · Cited by 13
Light‐Triggered CRISPR/Cas12a for Genomic Editing and Tumor Regression
Liu, H., Dong, J., Wu, R., Dai, J., Lou, X., Xia, F., Willner, I., & Huang, F. (2025) · Angewandte Chemie International Edition · doi:10.1002/anie.202502892 · Cited by 12
Potential clinical treatment prospects behind the molecular mechanism of alternative lengthening of telomeres (ALT)
Sun, H., Chen, G., Guo, B., Lv, S., & Yuan, G. (2023) · Journal of Cancer · doi:10.7150/jca.80097 · Cited by 11
DNA-PK participates in pre-rRNA biogenesis independent of DNA double-strand break repair
Li, P., Gai, X., Li, Q., Yang, Q., & Yu, X. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae316 · Cited by 11
Shining light on CRISPR/Cas9 therapeutics for inherited retinal diseases
Geiger, A., Kennedy, J. G., Staker, L. G., Wensel, T. G., Casson, R. J., & Thomas, P. Q. (2025) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2025.101376 · Cited by 11
Long-read sequencing reveals pre-meiotic gene conversion in sperm
Schweiger, R., Lee, S. Y., Zhou, C., Yang, T.-P., Li, S., Sanghvi, R., Neville, M. D. C., Smith, K., Roberts, K., Nessa, A., et al. (2026) · Nature · doi:10.1038/s41586-026-10901-0 · Cited by 14
High-LET Proton Irradiation Significantly Alters the Clonogenic and Tumorigenic Potential of Human Breast Cancer Cell Lines In Vitro and In Vivo
Pustovalova, M. V., Mohammad, R., Wang, Y., Xue, W., Malakhov, P., Nekrasov, V., Kontareva, E., Nofal, Z., Saburov, V. O., Kolesov, D. V., et al. (2025) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl36415 · Cited by 10
Pyridine-bis(benzimidazole) induces DNA damage at G-quadruplex loci and promotes synthetic lethality with DNA repair inhibition
Yan, J., Bu, L., Wang, Y., Yao, H., Li, G., Zheng, K., & Huang, J. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf543 · Cited by 10
Proximal binding of dCas9 at a DNA double strand break stimulates homology-directed repair as a local inhibitor of classical non-homologous end joining
Feng, Y.-L., Liu, S., Chen, R.-D., Sun, X., Xiao, J., Xiang, J.-F., & Xie, A. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad116 · Cited by 10
CRISPR applications in microbial World: Assessing the opportunities and challenges
Kursheed, F., Naz, E., Mateen, S., & Kulsoom, U. (2024) · Gene · doi:10.1016/j.gene.2024.149075 · Cited by 10
The Role of SWI / SNF Complex in Bladder Cancer
Lei, Z., Han, Y., Liao, J., Li, X., Su, Q., & Yang, Z. (2025) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.70348 · Cited by 9
DNA damage response signatures are associated with frontline chemotherapy response and routes of tumor evolution in extensive stage small cell lung cancer
Morris, B. B., Heeke, S., Xi, Y., Diao, L., Wang, Q., Rocha, P., Arriola, E., Lee, M. C., Tyson, D. R., Concannon, K., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02291-0 · Cited by 9
The mammalian Ku70 C-terminus SAP domain is required to repair DNA damage
Wang, Y., Czap, M. S., Kim, H., Masaka, P. M., Wang, H., Beg, M. A., Lu, H., Liu, J., Chang, Y., Romanienko, P. J., et al. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf499 · Cited by 9
DNA Damage and Repair in Thyroid Physiology and Disease
Arczewska, K. D., Sys, D., Nilsen, H. L., & Piekiełko‐Witkowska, A. (2025) · Endocrine Reviews · doi:10.1210/endrev/bnaf035 · Cited by 9
CRISPR/cas genome editing for neurodegenerative diseases: Mechanisms, therapeutic advances, and clinical prospects
Pandya, K., & Kumar, D. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102922 · Cited by 9
The emerging impact of CRISPR and gene editing on global crop improvement
Mansi, M., & Danai, P. (2026) · Transgenic Research · doi:10.1007/s11248-026-00484-x · Cited by 12
DNA polymerases in precise and predictable CRISPR/Cas9-mediated chromosomal rearrangements
Mehryar, M. M., Shi, X., Li, J., & Wu, Q. (2023) · BMC Biology · doi:10.1186/s12915-023-01784-y · Cited by 9
DNA-PK: A synopsis beyond synapsis
Goff, N. J., Mikhova, M., Schmidt, J. C., & Meek, K. (2024) · DNA repair · doi:10.1016/j.dnarep.2024.103716 · Cited by 9
A transposase-derived gene required for human brain development
Jubierre, L., Lewis, S. A., Gutierrez, R. L., Yamada, M., Rodríguez-Fos, E., Planas-Fèlix, M., Cameron, D., Demarest, P., Nabila, A., Mueller, H., et al. (2026) · Science Advances · doi:10.1126/sciadv.adv7530 · Cited by 9
Molecular dynamics of DNA repair and carcinogen interaction: Implications for cancer initiation, progression, and therapeutic strategies
Alyafeai, E., Qaed, E., Al-mashriqi, H. S., Al‐Maamari, A., Almansory, A. H., Futini, F. A., Sultan, M., & Tang, Z. (2024) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2024.111883 · Cited by 10
A Gemini Virus-Derived Autonomously Replicating System for HDR-Mediated Genome Editing of the EPSP Synthase Gene in Indica Rice
Borphukan, B., Khatun, M., Fartyal, D., James, D., & Reddy, M. K. (2025) · Plants · doi:10.3390/plants14030477 · Cited by 8
Evidence of requirement for homologous‐mediated DNA repair during Ambystoma mexicanum limb regeneration
García‐Lepe, U. O., Torres‐Dimas, E., Espinal‐Centeno, A., Cruz‐Ramírez, A., & Bermúdez‐Cruz, R. M. (2022) · Developmental Dynamics · doi:10.1002/dvdy.455 · Cited by 9
Gene therapy strategies for RAG1 deficiency: Challenges and breakthroughs
Gilioli, G., Lankester, A. C., de Kivit, S., Staal, F. J. T., & de Bruin, L. M. O. (2024) · Immunology Letters · doi:10.1016/j.imlet.2024.106931 · Cited by 8
TREX2 enables efficient genome disruption mediated by paired CRISPR-Cas9 nickases that generate 3′-overhanging ends
Wang, Y., Feng, Y.-L., Liu, Q., Xiao, J., Liu, S., Huang, Z., & Xie, A. (2023) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2023.102072 · Cited by 8
Cold snapshots of DNA repair: Cryo-EM structures of DNA-PKcs and NHEJ machinery
Amin, H., Zahid, S., Hall, C., & Chaplin, A. K. (2023) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2023.11.007 · Cited by 8
Proteins Associated with Neurodegenerative Diseases: Link to DNA Repair
Khodyreva, S. N., Dyrkheeva, N. S., & Lavrik, O. I. (2024) · Biomedicines · doi:10.3390/biomedicines12122808 · Cited by 7
ARID1A stabilizes non-homologous end joining factors at DNA breaks induced by the G4 ligand pyridostatin
Simoes‐Sousa, S., Amin, N., Lane, K. A., Harrod, A., Pedersen, M., Pardo, M., Rasetti‐Escargueil, C., Kozik, Z., Begg, K., Ribeiro, A., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116277 · Cited by 7
SUMOylation is destined for regulatory T cell-related immune dysregulation
Qian, J., Yu, L., Tian, M., Li, X., Bai, X., Yang, J., Deng, R., Liu, Q., Lü, A., Xiao, C., et al. (2026) · Cell Death Discovery · doi:10.1038/s41420-026-02946-x · Cited by 7
Single-molecule fluorescence imaging techniques reveal molecular mechanisms underlying deoxyribonucleic acid damage repair
Kang, Y., An, S., Min, D., & Lee, J. Y. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.973314 · Cited by 7
Application and progress of CRISPR/Cas9 gene editing in B-cell lymphoma: a narrative review
Jin, Y., Wu, H., Liu, J., Cho, W. C. S., & Song, G. (2024) · Translational Cancer Research · doi:10.21037/tcr-23-1146 · Cited by 7
KDM7A-DT induces genotoxic stress, tumorigenesis, and progression of p53 missense mutation-associated invasive breast cancer
Giannakakis, A., Tsifintaris, M., Gouzouasis, V., Ow, G. S., Aau, M. Y., Papp, C., Ivshina, A. V., & Kuznetsov, V. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1227151 · Cited by 7
Replicative Instability Drives Cancer Progression
Morris, B. B., Smith, J. P., Zhang, Q., Jiang, Z., Hampton, O. A., Churchman, M. L., Arnold, S. M., Owen, D. H., Gray, J. E., Dillon, P. M., et al. (2022) · Biomolecules · doi:10.3390/biom12111570 · Cited by 7
The role of RNF138 in DNA end resection is regulated by ubiquitylation and CDK phosphorylation
Locke, A. J., Farraj, R. A., Tran, C., Zeinali, E., Mashayekhi, F., Ali, J. Y. H., Glover, J. N. M., & Ismail, I. H. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.105709 · Cited by 6
Emerging connections: Poly(ADP-ribose), FET proteins and RNA in the regulation of DNA damage condensates
Lombardi, S., Zilocchi, M., Nicsanu, R., & Barabino, S. M. L. (2025) · DNA repair · doi:10.1016/j.dnarep.2025.103846 · Cited by 6
Advancing Genotoxicity Assessment by Building a Global AOP Network
Demuynck, E., Vanhaecke, T., Thienpont, A., Cappoen, D., Goethem, F. V., Winkelman, L. M. T., Beltman, J. B., Murugadoss, S., Olsen, A.-K. H., Marcon, F., et al. (2025) · Environmental and Molecular Mutagenesis · doi:10.1002/em.70022 · Cited by 6

Authors: Stinson, B. M., & Loparo, J. J.
Affiliations: Harvard University (US)
Corresponding author: Loparo, Joseph J.
ORCID: Stinson, Benjamin M.
Loparo, Joseph J.
Venue: Annual Review of Biochemistry
Publisher: Annual Reviews
Published: 2021-06-20
Volume: 90
Issue: 1
Pages: 137-164
ISSN: 0066-4154 (ISSN-L)
1545-4509
DOI: 10.1146/annurev-biochem-080320-110356
PMC: PMC8899865
OpenAlex: W3127347270
Cited by: 223
References: 173
Citations by year: 2026: 49 · 2025: 61 · 2024: 57 · 2023: 33 · 2022: 19 · 2021: 4
FWCI: 3.04
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Annual Review of Biochemistry (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Damon Runyon Cancer Research Foundation
National Institutes of Health
National Institute of General Medical Sciences (R01GM115487)
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: non-homologous end joining, DNA double-strand breaks, DNA end processing, genome stability, chromosomal translocation, DNA ligation
MeSH terms: Animals, Enzymes, Humans, Models, Biological, Genomic Instability, Multiprotein Complexes, DNA Breaks, Double-Stranded, DNA End-Joining Repair, V(D)J Recombination

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Repair of DNA Double-Strand Breaks by the Nonhomologous End Joining Pathway

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks