DNA double-strand break repair: From mechanistic understanding to cancer treatment
Abstract
Accurate repair of DNA double-strand breaks is essential to life. Indeed, defective DNA double-strand break repair can lead to toxicity and large scale sequence rearrangements that cause cancer and promote premature aging. Here, we highlight the two major repair systems for handling DNA double-strand breaks: homologous recombination and non-homologous end joining. To clarify recombination mechanisms, we present animations that illustrate DNA strand movements. In addition to describing how these pathways operate, we also describe why appropriate pathway choice is critical to genomic stability, and we summarize key pathway control features related to cell cycle checkpoint and apoptosis signaling. Importantly, recent progress in delineating the effects of specific defects in repair and checkpoint control has helped to explain several disease phenotypes, including cancer and premature aging. Improved understanding of these pathways has also sparked development of novel chemotherapeutic strategies that kill tumors with increased specificity and efficacy. This review aims to provide a foundational understanding of how the homologous recombination and non-homologous end joining pathways operate, and to demonstrate how a better understanding of these processes has advanced both our understanding of the underlying causes of cancer and our ability to innovate novel cancer treatment strategies.
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RAD51 works together with BRCA2 to allow strand invasion onto an undamaged DNA duplex.
“In this step, RAD51 works together with BRCA2 to allow the strand invasion onto undamaged DNA duplex [119,120].”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [119]
Cites
Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy
Farmer, H., McCabe, N., Lord, C. J., Tutt, A. N. J., Johnson, D. A., Richardson, T. B., Santarosa, M., Dillon, K. J., Hickson, I., Knights, C., et al. (2005) · Nature · doi:10.1038/nature03445 · Cited by 6,683 · see citing works
Instability and decay of the primary structure of DNA
Lindahl, T. (1993) · Nature · doi:10.1038/362709a0 · Cited by 5,679 · see citing works
Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase
Bryant, H. E., Schultz, N., Thomas, H. D., Parker, K. M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N. J., & Helleday, T. (2005) · Nature · doi:10.1038/nature03443 · Cited by 5,198 · see citing works
Self-citationThe double-strand-break repair model for recombination
Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J., & Stahl, F. W. (1983) · Cell · doi:10.1016/0092-8674(83)90331-8 · Cited by 2,437 · see citing works
Alu repeats and human genomic diversity
Batzer, M., & Deininger, P. (2002) · Nature reviews genetics · doi:10.1038/nrg798 · Cited by 1,522 · see citing works
Brca1 Controls Homology-Directed DNA Repair
Moynahan, M. E., Chiu, J. W., Koller, B. H., & Jasin, M. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80202-6 · Cited by 1,245 · see citing works
Chromosomal stability and the DNA double-stranded break connection
van Gent, D. C., Hoeijmakers, J. H. J., & Kanaar, R. (2001) · Nature Reviews Genetics · doi:10.1038/35056049 · Cited by 1,219 · see citing works
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 · see citing works
Pathways of DNA Double-Strand Break Repair during the Mammalian Cell Cycle
Rothkamm, K., Krüger, I., Thompson, L. H., & Lübrich, M. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.16.5706-5715.2003 · Cited by 1,187 · see citing works
Ma, Y., Pannicke, U., Schwarz, K., & Lieber, M. R. (2002) · Cell · doi:10.1016/s0092-8674(02)00671-2 · Cited by 1,166 · see citing works
A mechanism for gene conversion in fungi
Holliday, R. (2007) · Genetics Research · doi:10.1017/s0016672308009476 · Cited by 1,144 · see citing works
The Bloom's syndrome helicase suppresses crossing over during homologous recombination
Wu, L., & Hickson, I. D. (2003) · Nature · doi:10.1038/nature02253 · Cited by 1,087 · see citing works
The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis
Falck, J., Mailand, N., Syljuåsen, R. G., Bartek, J., & Lukas, J. (2001) · Nature · doi:10.1038/35071124 · Cited by 1,085 · see citing works
Requirement of the MRN complex for ATM activation by DNA damage
Uziel, T., Lerenthal, Y., Moyal, L., Andegeko, Y., Mittelman, L., & Shiloh, Y. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg541 · Cited by 1,075 · see citing works
Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells
Murcia, J. M., Niedergang, C., Trucco, C., Ricoul, M., Dutrillaux, B., Mark, M. P., Oliver, F. J., Masson, M., Dierich, A., LeMeur, M., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7303 · Cited by 1,058 · see citing works
The importance of repairing stalled replication forks
Cox, M. M., Goodman, M. F., Kreuzer, K. N., Sherratt, D. J., Sandler, S. J., & Marians, K. J. (2000) · Nature · doi:10.1038/35003501 · Cited by 1,044 · see citing works
BRCA2 Is Required for Homology-Directed Repair of Chromosomal Breaks
Moynahan, M. E., Pierce, A. J., & Jasin, M. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00174-5 · Cited by 1,007 · see citing works
A Manyfold Increase in Sister Chromatid Exchanges in Bloom's Syndrome Lymphocytes
Chaganti, R. S. K., Schonberg, S. A., & GERMAN, J. L. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.11.4508 · Cited by 947 · see citing works
The 3′ to 5′ Exonuclease Activity of Mre11 Facilitates Repair of DNA Double-Strand Breaks
Paull, T. T., & Gellert, M. F. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80097-0 · Cited by 919 · see citing works
Moshous, D., Callebaut, I., de Chasseval, R., Corneo, B., Cavazzana, M., Deist, F. L., Tezcan, İ., Sanal, Ö., Bertrand, Y., Philippe, N., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00309-9 · Cited by 912 · see citing works
Rad51‐deficient vertebrate cells accumulate chromosomal breaks prior to cell death
Sonoda, E., Sasaki, M., Buerstedde, J., Bezzubova, O., Shinohara, A., Ogawa, H., Takata, M., Yamaguchi-Iwai, Y., & Takeda, S. (1998) · EMBO Journal · doi:10.1093/emboj/17.2.598 · Cited by 860 · see citing works
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 · see citing works
The Fanconi anaemia/BRCA pathway
D'Andrea, A. D., & Grompe, M. (2003) · Nature Reviews Cancer · doi:10.1038/nrc970 · Cited by 822 · see citing works
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 · see citing works
Targeted disruption of the Rad51 gene leads to lethality in embryonic mice.
Tsuzuki, T., Fujii, Y., Sakumi, K., Tominaga, Y., Nakao, K., Sekiguchi, M., Matsushiro, A., Yoshimura, Y., & MoritaT (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.13.6236 · Cited by 792 · see citing works
DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1
Ira, G., Pellicioli, A., Balijja, A., Wang, X., Fiorani, S., Carotenuto, W., Liberi, G., Bressan, D., Wan, L., Hollingsworth, N. M., et al. (2004) · Nature · doi:10.1038/nature02964 · Cited by 722 · see citing works
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 · see citing works
Role of BRCA2 in Control of the RAD51 Recombination and DNA Repair Protein
Davies, A. A., Masson, J., McIlwraith, M. J., Stasiak, A. Z., Stasiak, A., Venkitaraman, A. R., & West, S. C. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00175-7 · Cited by 720 · see citing works
Human Rad51 Protein Promotes ATP-Dependent Homologous Pairing and Strand Transfer Reactions In Vitro
Baumann, P., Benson, F. E., & West, S. C. (1996) · Cell · doi:10.1016/s0092-8674(00)81394-x · Cited by 689 · see citing works
Lim, D., & Hasty, P. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.12.7133 · Cited by 687 · see citing works
Involvement of Brca2 in DNA Repair
Patel, K. J., Yu, V. P. C. C., Lee, H., Corcoran, A. E., Thistlethwaite, F. C., Evans, M. J., Colledge, W. H., Friedman, L. S., Ponder, B. A. J., & Venkitaraman, A. R. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80035-0 · Cited by 631 · see citing works
The origin of interspersed repeats in the human genome
Smit, A. F. A. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80030-x · Cited by 611 · see citing works
A loss-of-function RNA interference screen for molecular targets in cancer
Ngo, V. N., Davis, R. E., Lamy, L., Yu, X., Zhao, H. G., Lenz, G., Lam, L. T., Davé, S. S., Yang, L., Powell, J. I., et al. (2006) · Nature · doi:10.1038/nature04687 · Cited by 606 · see citing works
The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases
Mohaghegh, P. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.13.2843 · Cited by 599 · see citing works
Johnson, R. D., & Jasin, M. (2000) · The EMBO Journal · doi:10.1093/emboj/19.13.3398 · Cited by 590 · see citing works
Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A
New, J. H., Sugiyama, T., Zaitseva, E., & Kowalczykowski, S. C. (1998) · Nature · doi:10.1038/34950 · Cited by 589 · see citing works
The role of double-strand break repair — insights from human genetics
O’Driscoll, M., & Jeggo, P. A. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1746 · Cited by 581 · see citing works
The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair
Hopfner, K., Craig, L., Moncalián, G., Zinkel, R. A., Usui, T., Owen, B. A. L., Kärcher, A., Henderson, B., Bodmer, J.-L., McMurray, C. T., et al. (2002) · Nature · doi:10.1038/nature00922 · Cited by 571 · see citing works
PARP is important for genomic stability but dispensable in apoptosisPreprint
Wang, Z., Stingl, L., Morrison, C. G., Jantsch, M. F., Łoś, M., Schulze‐Osthoff, K., & Wagner, E. F. (1997) · Genes & Development · doi:10.1101/gad.11.18.2347 · Cited by 557 · see citing works
Syljuåsen, R. G., Sørensen, C. S., Hansen, L. T., Fugger, K., Lundin, C., Johansson, F., Helleday, T., Sehested, M., Lukas, J., & Bártek, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.9.3553-3562.2005 · Cited by 550 · see citing works
Self-citationFrequent chromosomal translocations induced by DNA double-strand breaks
Richardson, C., & Jasin, M. (2000) · Nature · doi:10.1038/35015097 · Cited by 517 · see citing works
Human Rad50/Mre11 Is a Flexible Complex that Can Tether DNA Ends
de Jager, M., van Noort, J., van Gent, D. C., Dekker, C., Kanaar, R., & Wyman, C. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00381-1 · Cited by 512 · see citing works
The Bloom's syndrome gene product promotes branch migration of Holliday junctions
Karow, J., Constantinou, A., Li, J., West, S. C., & Hickson, I. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.100448097 · Cited by 502 · see citing works
Niedernhofer, L. J., Odijk, H., Budzowska, M., van Drunen, E., Maas, A., Theil, A. F., de Wit, J., Jaspers, N. G. J., Beverloo, H. B., Hoeijmakers, J. H. J., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.13.5776-5787.2004 · Cited by 493 · see citing works
Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins
Petukhova, G. D., Stratton, S. A., & Sung, P. (1998) · Nature · doi:10.1038/30037 · Cited by 445 · see citing works
Richardson, C. A., Moynahan, M. E., & Jasin, M. (1998) · Genes & Development · doi:10.1101/gad.12.24.3831 · Cited by 442 · see citing works
Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4
Mari, P., Florea, B. I., Persengiev, S. P., Verkaik, N. S., Brüggenwirth, H. T., Modesti, M., Giglia‐Mari, G., Bezstarosti, K., Demmers, J., Luider, T. M., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609061103 · Cited by 423 · see citing works
Recombinational DNA repair and human disease
Thompson, L. H., & Schild, D. (2002) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/s0027-5107(02)00224-5 · Cited by 417 · see citing works
Clarifying the mechanics of DNA strand exchange in meiotic recombination
Neale, M. J., & Keeney, S. (2006) · Nature · doi:10.1038/nature04885 · Cited by 417 · see citing works
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 · see citing works
Identification and purification of two distinct complexes containing the five RAD51 paralogsPreprint
Masson, J., Tarsounas, M., Stasiak, A. Z., Stasiak, A., Punatar, R. S., McIlwraith, M. J., Benson, F. E., & West, S. C. (2001) · Genes & Development · doi:10.1101/gad.947001 · Cited by 395 · see citing works
The CDK regulates repair of double‐strand breaks by homologous recombination during the cell cycle
Aylon, Y., Liefshitz, B., & Kupiec, M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600469 · Cited by 387 · see citing works
Arnaudeau, C., Lundin, C., & Helleday, T. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4564 · Cited by 387 · see citing works
Self-citationConstantinou, A., Tarsounas, M., Karow, J., Brosh, R. M., Bohr, V. A., Hickson, I. D., & West, S. C. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd004 · Cited by 387 · see citing works
ATR and ATM regulate the timing of DNA replication origin firing
Shechter, D., Costanzo, V., & Gautier, J. (2004) · Nature Cell Biology · doi:10.1038/ncb1145 · Cited by 383 · see citing works
Cancer predisposition caused by elevated mitotic recombination in Bloom mice
Luo, G., Santoro, I. Μ., McDaniel, L. D., Nishijima, I., Mills, M., Youssoufian, H., Vogel, H. S., Schultz, R. A., & Bradley, A. (2000) · Nature Genetics · doi:10.1038/82548 · Cited by 372 · see citing works
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 · see citing works
The exaptive excellence of spandrels as a term and prototype
Gould, S. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10750 · Cited by 346 · see citing works
Shao, R.-G., Cao, C., Zhang, H., Kohn, K. W., Wold, M. S., & Pommier, Y. (1999) · The EMBO Journal · doi:10.1093/emboj/18.5.1397 · Cited by 345 · see citing works
Saleh-Gohari, N., Bryant, H. E., Schultz, N., Parker, K. M., Cassel, T. N., & Helleday, T. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7158-7169.2005 · Cited by 334 · see citing works
Self-citationMcElhinny, 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 · see citing works
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 · see citing works
Thompson, L. H., Brookman, K. W., Dillehay, L. E., Carrano, A. V., Mazrimas, J. A., Mooney, C. L., & Minkler, J. L. (1982) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(82)90276-7 · Cited by 321 · see citing works
Gene Conversion Tracts from Double-Strand Break Repair in Mammalian Cells
Elliott, B., Richardson, C. A., Winderbaum, J., Nickoloff, J. A., & Jasin, M. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.1.93 · Cited by 305 · see citing works
McIlwraith, M. J., Vaisman, A., Liu, Y., Fanning, E., Woodgate, R., & West, S. C. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.10.001 · Cited by 304 · see citing works
Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination
Schultz, N. D. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg703 · Cited by 301 · see citing works
Damage recognition in nucleotide excision repair of DNA
Batty, D. P., & Wood, R. D. (2000) · Gene · doi:10.1016/s0378-1119(99)00489-8 · Cited by 296 · see citing works
Rescue of arrested replication forks by homologous recombination
Michel, B., Flores, M. J., Viguera, E., Grompone, G., Seigneur, M., & Bidnenko, V. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111008798 · Cited by 292 · see citing works
Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA
Moreno‐Herrero, F., de Jager, M., Dekker, N. H., Kanaar, R., Wyman, C., & Dekker, C. (2005) · Nature · doi:10.1038/nature03927 · Cited by 278 · see citing works
Chappell, C., Hanakahi, L. A., Karimi‐Busheri, F., Weinfeld, M., & West, S. C. (2002) · The EMBO Journal · doi:10.1093/emboj/21.11.2827 · Cited by 275 · see citing works
Sargent, R. G., Brenneman, M. A., & Wilson, J. H. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.1.267 · Cited by 271 · see citing works
der Zwet, M. K.-V., Overkamp, W. J., van Lange, R. E. E., Essers, J., van Duijn-Goedhart, A., Wiggers, I., Swaminathan, S., van Buul, P. V., Errami, A., Tan, R., et al. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.2.669-679.2002 · Cited by 267 · see citing works
Mediator function of the human Rad51B–Rad51C complex in Rad51/RPA-catalyzed DNA strand exchangePreprint
Sigurðsson, S., Komen, S. V., Bussen, W., Schild, D., Albala, J. S., & Sung, P. (2001) · Genes & Development · doi:10.1101/gad.935501 · Cited by 257 · see citing works
Homologous Recombination Resolution Defect in Werner Syndrome
Saintigny, Y., Makienko, K., Swanson, C. L., Emond, M. J., & Monnat, R. J. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.20.6971-6978.2002 · Cited by 257 · see citing works
Sugiyama, T., & Kowalczykowski, S. C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203494200 · Cited by 251 · see citing works
Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells
Kim, J. S., Krasieva, T. B., Kurumizaka, H., Chen, D. J., Taylor, A. M. R., & Yokomori, K. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200411083 · Cited by 248 · see citing works
Mre11 Protein Complex Prevents Double-Strand Break Accumulation during Chromosomal DNA Replication
Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., & Gautier, J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00294-5 · Cited by 239 · see citing works
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 · see citing works
The mechanism of non-homologous end-joining: a synopsis of synapsis
Weterings, E., & van Gent, D. C. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.06.003 · Cited by 235 · see citing works
Li, G. C., Ouyang, H., Li, X., Nagasawa, H., Little, J. B., Chen, D. J., Ling, C., FUKS, Z. Y., & Cordon-Cardo, C. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80108-2 · Cited by 233 · see citing works
Break-induced replication: A review and an example in budding yeast
Kraus, E., Leung, W.-Y., & Haber, J. E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151008198 · Cited by 233 · see citing works
Dual Roles for DNA Polymerase η in Homologous DNA Recombination and Translesion DNA Synthesis
Kawamoto, T., Araki, K., Sonoda, E., Yamashita, Y. M., Harada, K. H., Kikuchi, K., Masutani, C., Hanaoka, F., Nozaki, K., Hashimoto, N., et al. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.10.016 · Cited by 231 · see citing works
Visualization of Altered Replication Dynamics after DNA Damage in Human Cells
Merrick, C. J., Jackson, D. A., & Diffley, J. F. X. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400022200 · Cited by 228 · see citing works
A Double Holliday Junction Dissolvasome Comprising BLM, Topoisomerase IIIα, and BLAP75
Raynard, S. J., Bussen, W., & Sung, P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.c600051200 · Cited by 227 · see citing works
Moshous, D., Pannetier, C., de Chasseval, R., Deist, F. L., Cavazzana, M., Romana, S. P., Macintyre, E. A., Canioni, D., Brousse, N., Fischer, A., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci16774 · Cited by 226 · see citing works
p53‐catalyzed annealing of complementary single‐stranded nucleic acids.
Oberosler, P., Hloch, P., Ramsperger, U., & Stahl, H. D. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05893.x · Cited by 224 · see citing works
Methylation-induced blocks to in vitro DNA replication
Larson, K. L., Sahm, J., Shenkar, R., & Bs, S. (1985) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(85)90103-4 · Cited by 223 · see citing works
BRCA2-dependent and independent formation of RAD51 nuclear foci
Tarsounas, M., Davies, D. C., & West, S. C. (2003) · Oncogene · doi:10.1038/sj.onc.1206263 · Cited by 205 · see citing works
Schreiber, V., Hunting, D. J., Trucco, C., Gowans, B. J., Grünwald, D., de MURCIA, G., & Murcia, J. M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.11.4753 · Cited by 203 · see citing works
Specific Interactions between the Human RAD51 and RAD52 Proteins
Shen, Z., Cloud, K. G., Chen, D. J., & Park, M. S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.1.148 · Cited by 200 · see citing works
Rad54 protein promotes branch migration of Holliday junctions
Bugreev, D. V., Mazina, O. M., & Mazin, A. V. (2006) · Nature · doi:10.1038/nature04889 · Cited by 195 · see citing works
Alu: Structure, Origin, Evolution, Significance, and Function of One-Tenth of Human DNA
Schmid, C. W. (1996) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)60148-8 · Cited by 193 · see citing works
Chromatin structural elements and chromosomal translocations in leukemia
Zhang, Y., & Rowley, J. D. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.020 · Cited by 184 · see citing works
Petermann, E., Maya‐Mendoza, A., Zachos, G., Gillespie, D. A., Jackson, D. A., & Caldecott, K. W. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.8.3319-3326.2006 · Cited by 183 · see citing works
Chromosomal Translocation Mechanisms at Intronic Alu Elements in Mammalian Cells
Elliott, B., Richardson, C. A., & Jasin, M. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.02.028 · Cited by 177 · see citing works
Sharpless, N. E., Ferguson, D. O., O’Hagan, R. C., Castrillón, D. H., Lee, C., Farazi, P. A., Alson, S., Fleming, J., Morton, C. C., Frank, K. M., et al. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00425-7 · Cited by 173 · see citing works
Petermann, E., & Caldecott, K. W. (2006) · Cell Cycle · doi:10.4161/cc.5.19.3256 · Cited by 163 · see citing works
WRN exonuclease structure and molecular mechanism imply an editing role in DNA end processing
Perry, J. J. P., Yannone, S. M., Holden, L. G., Hitomi, C., Asaithamby, A., Han, S., Cooper, P. K., Chen, D. J., & Tainer, J. A. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1088 · Cited by 158 · see citing works
Human p53 Binds Holliday Junctions Strongly and Facilitates Their Cleavage
Lee, S., Cavallo, L. M., & Griffith, J. D. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.11.7532 · Cited by 152 · see citing works
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 · see citing works
Prado, F., & Aguilera, A. (1995) · Genetics · doi:10.1093/genetics/139.1.109 · Cited by 129 · see citing works
Engelward, B. P., Allan, J. M., Dreslin, A. J., Kelly, J. D., Wu, M. M., Gold, B. I., & Samson, L. D. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.9.5412 · Cited by 128 · see citing works
Self-citationRole of ERCC1 in removal of long non‐homologous tails during targeted homologous recombination
Adair, G. M., Rolig, R. L., Moore‐Faver, D., Zabelshansky, M., Wilson, J. H., & Nairn, R. S. (2000) · The EMBO Journal · doi:10.1093/emboj/19.20.5552 · Cited by 125 · see citing works
Evidence for intrachromosomal gene conversion in cultured mouse cells
Liskay, R. M., & Stachelek, J. L. (1983) · Cell · doi:10.1016/0092-8674(83)90218-0 · Cited by 125 · see citing works
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 · see citing works
Extensive Loss of Heterozygosity Is Suppressed during Homologous Repair of Chromosomal Breaks
Stark, J. M., & Jasin, M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.23.2.733-743.2003 · Cited by 122 · see citing works
High frequency in vivo loss of heterozygosity is primarily a consequence of mitotic recombination.
Gupta, P. K., Sahota, A. S., Boyadjiev, S. A., Bye, S., Shao, C., O’Neill, J. P., Hunter, T., Albertini, R. J., Stambrook, P. J., & Tischfield, J. A. (1997) · PubMed · Cited by 117 · see citing works
RAD51 is involved in repair of damage associated with DNA replication in mammalian cells
Lundin, C., Schultz, N., Arnaudeau, C., Mohindra, A., Hansen, L. T., & Helleday, T. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00313-9 · Cited by 113 · see citing works
Self-citationBerger, J. M., & Schoeffler, A. J. (2005) · Biochemical Society Transactions · doi:10.1042/bst20051465 · Cited by 112 · see citing works
Simbulan-Rosenthal, C. M., Haddad, B. R., Rosenthal, D. S., Ohler, Z. W., Coleman, A., Luo, R., Young, H. M., Wang, Z., Ried, T., & Smulson, M. E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13191 · Cited by 105 · see citing works
Mechanisms of loss of heterozygosity in retinoblastoma
Zhu, X., Dunn, J. M., Goddard, A. D., Squire, J. A., Becker, A., Phillips, R. A., & Gallie, B. L. (2008) · Cytogenetics and Cell Genetics · doi:10.1159/000133261 · Cited by 105 · see citing works
The incidence of sister chromatid exchanges in cultured human lymphocytes
Morgan, W. F., & Crossen, P. E. (1977) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(77)80032-8 · Cited by 104 · see citing works
Gebow, D., Miselis, N. R., & Liber, H. L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4028-4035.2000 · Cited by 98 · see citing works
ATM is required for the cellular response to thymidine induced replication fork stress
Bolderson, E., Scorah, J., Helleday, T., Smythe, C., & Meuth, M. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh316 · Cited by 86 · see citing works
Self-citationvan Heemst, D., Brugmans, L., Verkaik, N. S., & van Gent, D. C. (2003) · DNA repair · doi:10.1016/j.dnarep.2003.09.004 · Cited by 83 · see citing works
Radiation effects on DNA synthesis in a defined chromosomal replicon.
Larner, J. M., Lee, H., & Hamlin, J. L. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.3.1901 · Cited by 79 · see citing works
Analysis of mouse Rad54 expression and its implications for homologous recombination
Essers, J., Hendriks, R. W., Wesoły, J., Beerens, C. E. M. T., Smit, B., Hoeijmakers, J. H. J., Wyman, C., Dronkert, M. L. G., & Kanaar, R. (2002) · DNA repair · doi:10.1016/s1568-7864(02)00110-6 · Cited by 79 · see citing works
Visualization of recombination intermediates produced by RAD52‐mediated single‐strand annealing
Dyck, E. V., Stasiak, A. Z., Stasiak, A., & West, S. C. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve201 · Cited by 78 · see citing works
Lucky breaks: analysis of recombination in Saccharomyces
Haber, J. E. (2000) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(00)00040-3 · Cited by 77 · see citing works
Molecular nature of in vivo mutations in human cells at the autosomal HLA-A locus.
Morley, A. A., Grist, S. A., Turner, D. R., Kutlaca, A., & Bennett, G. (1990) · PubMed · Cited by 72 · see citing works
Transpositions and translocations induced by site-specific double-strand breaks in budding yeast
Haber, J. E. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.025 · Cited by 70 · see citing works
Holmquist, G. P. (1998) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(98)00051-7 · Cited by 64 · see citing works
Rad52 and Ku bind to different DNA structures produced early in double-strand break repair
Ristić, D. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg729 · Cited by 58 · see citing works
Interactions between p53, hMSH2-hMSH6 and HMG I(Y) on Holliday junctions and bulged bases
Subramanian, D. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.11.2427 · Cited by 47 · see citing works
Construction of humanXRCC1minigenes that fully correct the CHO DNA repair mutant EM9
Caldecott, K. W., Tucker, J. D., & Thompson, L. H. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.17.4575 · Cited by 47 · see citing works
Lebel, M. (2002) · Carcinogenesis · doi:10.1093/carcin/23.1.213 · Cited by 39 · see citing works
Wiktor‐Brown, D. M., Hendricks, C. A., Olipitz, W., & Engelward, B. P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604943103 · Cited by 38 · see citing works
Self-citationOverkamp, W. J. I., Rooimans, M. A., Neuteboom, I., Telleman, P., Arwert, F., & Zdzienicka, M. Z. (1993) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01233248 · Cited by 35 · see citing works
The genetics of pancreatic adenocarcinoma: a roadmap for a mouse model
Bardeesy, N. M., Sharpless, N. E., DePinho, R. A., & Merlino, G. T. (2001) · Seminars in Cancer Biology · doi:10.1006/scbi.2000.0371 · Cited by 35 · see citing works
Jonnalagadda, V. S., Matsuguchi, T., & Engelward, B. P. (2005) · DNA repair · doi:10.1016/j.dnarep.2005.02.002 · Cited by 28 · see citing works
Self-citationV(D)J Recombination: Links to Transposition and Double-strand Break RepairPreprint
Gellert, M. F., Hesse, J. E., Hiom, K. J., Melek, M., Modesti, M., Paull, T. T., Ramsden, D. A., & van Gent, D. C. (1999) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1999.64.161 · Cited by 27 · see citing works
Saleh-Gohari, N., & Helleday, T. (2004) · Oncogene · doi:10.1038/sj.onc.1208178 · Cited by 17 · see citing works
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DNA repair pathways as targets for cancer therapy
Helleday, T., Petermann, E., Lundin, C., Hodgson, B., & Sharma, R. A. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2342 · Cited by 1,666 · see citing works
Self-citationHypoxic microenvironment in cancer: molecular mechanisms and therapeutic interventions
Chen, Z., Han, F., Du, Y., Shi, H., & Zhou, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01332-8 · Cited by 1,612 · see citing works
Hypoxia, DNA repair and genetic instability
Bristow, R. G., & Hill, R. P. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2344 · Cited by 1,140 · see citing works
Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining
Mahaney, B. L., Meek, K., & Lees‐Miller, S. P. (2009) · Biochemical Journal · doi:10.1042/bj20080413 · Cited by 723 · see citing works
Base excision repair of oxidative DNA damage and association with cancer and aging
Maynard, S., Schurman, S. H., Harboe, C., de Souza-Pinto, N. C., & Bohr, V. A. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn250 · Cited by 685 · see citing works
Factors determining DNA double‐strand break repair pathway choice in G2 phase
Shibata, A., Conrad, S., Birraux, J., Geuting, V., Barton, O., Ismail, A., Kakarougkas, A., Meek, K., Taucher-Scholz, G., Löbrich, M., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.27 · Cited by 481 · see citing works
DNA Damage ResponsePreprint
Giglia‐Mari, G., Zotter, A., & Vermeulen, W. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000745 · Cited by 487 · see citing works
Inflammation-induced DNA damage, mutations and cancer
Kay, J. E., Thadhani, E., Samson, L. D., & Engelward, B. P. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.102673 · Cited by 481 · see citing works
Self-citationDNA repair mechanisms in cancer development and therapy
Torgovnick, A., & Schumacher, B. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00157 · Cited by 403 · see citing works
Karanam, K., Kafri, R., Loewer, A., & Lahav, G. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.052 · Cited by 393 · see citing works
Mladenov, E., & Iliakis, G. E. (2011) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2011.02.005 · Cited by 381 · see citing works
Thompson, L. H. (2012) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2012.06.002 · Cited by 357 · see citing works
DNA repair deficiency in neurodegeneration
Jeppesen, D. K., Bohr, V. A., & Stevnsner, T. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.04.013 · Cited by 349 · see citing works
Ferguson, L. R., Chen, H., Collins, A. R., Connell, M., Damia, G. L. M., Dasgupta, S., Malhotra, M., Meeker, A. K., Amedei, A., Amin, A., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.03.005 · Cited by 340 · see citing works
Chan, N. H. L., Koritzinsky, M., Zhao, H. W., Bindra, R. S., Glazer, P. M., Powell, S. N., Belmaaza, A., Wouters, B. G., & Bristow, R. G. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5472 · Cited by 328 · see citing works
DNA repair deficiency and neurological disease
McKinnon, P. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2559 · Cited by 323 · see citing works
Akt: A Double-Edged Sword in Cell Proliferation and Genome Stability
Xu, N., Lao, Y., Zhang, Y., & Gillespie, D. A. (2012) · Journal of Oncology · doi:10.1155/2012/951724 · Cited by 308 · see citing works
ERCC1-XPF Endonuclease Facilitates DNA Double-Strand Break Repair
Ahmad, A., Robinson, A. R., Duensing, A. U., van Drunen, E., Beverloo, H. B., Weisberg, D. B., Hasty, P., Hoeijmakers, J. H. J., & Niedernhofer, L. J. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00293-08 · Cited by 298 · see citing works
Novel pro- and anti-recombination activities of the Bloom’s syndrome helicasePreprint
Bugreev, D. V., Yu, X., Egelman, E. H., & Mazin, A. V. (2007) · Genes & Development · doi:10.1101/gad.1609007 · Cited by 297 · see citing works
Mladenov, E., Magin, S., Soni, A., & Iliakis, G. E. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00113 · Cited by 292 · see citing works
DNA Damage Induced by Alkylating Agents and Repair Pathways
Kondo, N., Takahashi, A., Ono, K., & Ohnishi, T. (2010) · Journal of Nucleic Acids · doi:10.4061/2010/543531 · Cited by 299 · see citing works
PCNA on the crossroad of cancer
Stoimenov, I., & Helleday, T. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370605 · Cited by 292 · see citing works
Self-citationHomologous recombination in cancer development, treatment and development of drug resistance
Helleday, T. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq064 · Cited by 288 · see citing works
Self-citationKwok, M., Davies, N., Agathanggelou, A., Smith, E., Oldreive, C., Petermann, E., Stewart, G. S., Brown, J., Lau, A., Pratt, G., et al. (2015) · Blood · doi:10.1182/blood-2015-05-644872 · Cited by 281 · see citing works
Oza, A. M., Tinker, A. V., Oaknin, A., Shapira‐Frommer, R., McNeish, I. A., Swisher, E. M., Ray-Coquard, I. L., Bell‐McGuinn, K. M., Coleman, R. L., O’Malley, D. M., et al. (2017) · Gynecologic Oncology · doi:10.1016/j.ygyno.2017.08.022 · Cited by 280 · see citing works
Single cell trapping and DNA damage analysis using microwell arrays
Wood, D. K., Weingeist, D. M., Bhatia, S. N., & Engelward, B. P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004056107 · Cited by 260 · see citing works
Self-citationDrew, Y., Mulligan, E. A., Vong, W., Thomas, H. D., Kahn, S., Kyle, S., Mukhopadhyay, A., Los, G., Hostomský, Z., Plummer, E. R., et al. (2010) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djq509 · Cited by 262 · see citing works
Kristeleit, R. S., Shapiro, G. I., Burris, H. A., Oza, A. M., LoRusso, P. M., Patel, M. R., Domchek, S. M., Balmañà, J., Drew, Y., Chen, L.-M., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-2796 · Cited by 244 · see citing works
Identification of Specific Inhibitors of Human RAD51 Recombinase Using High-Throughput Screening
Huang, F., Motlekar, N. A., Burgwin, C. M., Napper, A. D., Diamond, S. L., & Mazin, A. V. (2011) · ACS Chemical Biology · doi:10.1021/cb100428c · Cited by 232 · see citing works
Hammel, M., Yu, Y., Mahaney, B. L., Cai, B., Ye, R., Phipps, B. M., Rambo, R. P., Hura, G. L., Pelikán, M., So, S., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.065615 · Cited by 230 · see citing works
The histone methyltransferase SET8 is required for S-phase progression
Jørgensen, S., Elvers, I., Trelle, M. B., Menzel, T., Eskildsen, M., Jensen, O. N., Helleday, T., Helin, K., & Sørensen, C. S. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200706150 · Cited by 225 · see citing works
Self-citationFOXM1: An emerging master regulator of DNA damage response and genotoxic agent resistance
Zona, S., Bella, L., Burton, M. J., de Moraes, G. N., & Lam, E. W. ‐. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.09.016 · Cited by 220 · see citing works
Electromagnetic fields and DNA damage
Phillips, J. L., Singh, N. P., & Lai, H. (2009) · Pathophysiology · doi:10.1016/j.pathophys.2008.11.005 · Cited by 226 · see citing works
Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response
Salton, M., Lerenthal, Y., Wang, S., Chen, D. J., & Shiloh, Y. (2010) · Cell Cycle · doi:10.4161/cc.9.8.11298 · Cited by 209 · see citing works
DNA Damage and Repair: From Molecular Mechanisms to Health Implications
Fabio Altieri, F., Grillo, C., Maceroni, M., & Chichiarelli, S. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1830 · Cited by 212 · see citing works
Understanding the limitations of radiation-induced cell cycle checkpoints
Deckbar, D., Jeggo, P. A., & Löbrich, M. (2011) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2011.575764 · Cited by 205 · see citing works
The therapeutic significance of mutational signatures from DNA repair deficiency in cancer
Ma, J., Setton, J. S., Lee, N. Y., Riaz, N., & Powell, S. N. (2018) · Nature Communications · doi:10.1038/s41467-018-05228-y · Cited by 192 · see citing works
Zeng, A., Wei, Z., Yan, W., Yin, J., Huang, X., Zhou, X., Li, R., Shen, F., Wu, W., Wang, X., et al. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.08.004 · Cited by 193 · see citing works
Recent Advances in Cancer Therapy Targeting Proteins Involved in DNA Double-Strand Break Repair
Bolderson, E., Richard, D. J., Zhou, B. S., & Khanna, K. K. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0096 · Cited by 185 · see citing works
The role of homologous recombination in radiation-induced double-strand break repair
Jeggo, P. A., Geuting, V., & Löbrich, M. (2011) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2011.06.019 · Cited by 184 · see citing works
Molecular targeting of hypoxia in radiotherapy
Rey, S., Schito, L., Koritzinsky, M., & Wouters, B. G. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2016.10.002 · Cited by 171 · see citing works
Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies
Kciuk, M., Marciniak, B., Mojzych, M., & Kontek, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197264 · Cited by 168 · see citing works
DNA Repair and Genome Maintenance in Bacillus subtilis
Lenhart, J. S., Schroeder, J. W., Walsh, B. W., & Simmons, L. A. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05020-11 · Cited by 165 · see citing works
Inflammation-Induced Cell Proliferation Potentiates DNA Damage-Induced Mutations In Vivo
Kiraly, O., Gong, G., Olipitz, W., Muthupalani, S., & Engelward, B. P. (2015) · PLOS Genetics · doi:10.1371/journal.pgen.1004901 · Cited by 169 · see citing works
Self-citationNon-homologous end-joining, a sticky affair
van Gent, D. C., & van der Burg, M. (2007) · Oncogene · doi:10.1038/sj.onc.1210871 · Cited by 163 · see citing works
Drew, Y., Ledermann, J. A., Hall, G. D., Rea, D. W., Glasspool, R. M., Highley, M., Jayson, G. C., Sludden, J., Murray, J., Jamieson, D., et al. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.41 · Cited by 161 · see citing works
Strozyk, E. A., & Kulms, D. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140815260 · Cited by 160 · see citing works
Oxidative stress at low levels can induce clustered DNA lesions leading to NHEJ mediated mutations
Sharma, V., Collins, L. B., Chen, T.-H., Herr, N. R., Takeda, S., Sun, W., Swenberg, J. A., & Nakamura, J. (2016) · Oncotarget · doi:10.18632/oncotarget.8298 · Cited by 159 · see citing works
Engineering Human Stem Cell Lines with Inducible Gene Knockout using CRISPR/Cas9
Chen, Y., Cao, J., Xiong, M., Petersen, A. J., Dong, Y. W., Tao, Y., Huang, C. T.-L., Du, Z., & Zhang, S. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.06.001 · Cited by 160 · see citing works
Douglas, P., Zhong, J., Ye, R., Moorhead, G. B. G., Xu, X., & Lees‐Miller, S. P. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00741-09 · Cited by 159 · see citing works
Watson, C., Ge, J., Cohen, J., Pyrgiotakis, G., Engelward, B. P., & Demokritou, P. (2014) · ACS Nano · doi:10.1021/nn404871p · Cited by 158 · see citing works
Self-citationTargeted therapies in gynecological cancers: a comprehensive review of clinical evidence
Wang, Q., Peng, H., Qi, X., Wu, M., & Zhao, X. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-0199-6 · Cited by 157 · see citing works
Shaked, H., Hofseth, L. J., Chumanevich, A. P., Chumanevich, A. A., Wang, J., Wang, Y., Taniguchi, K., Gumá, M., Shenouda, S., Clevers, H. C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211509109 · Cited by 151 · see citing works
Rai, P., Parrish, M. C., Tay, I. J. J., Li, N., Ackerman, S., He, F., Kwang, J., Chow, V. T. K., & Engelward, B. P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424144112 · Cited by 145 · see citing works
Self-citationJames, D. I., Smith, K. M., Jordan, A. M., Fairweather, E. E., Griffiths, L. A., Hamilton, N. S., Hitchin, J. R., Hutton, C. P., Jones, S. D., Kelly, P. J., et al. (2016) · ACS Chemical Biology · doi:10.1021/acschembio.6b00609 · Cited by 143 · see citing works
Inhibition of Homologous Recombination in Human Cells by Targeting RAD51 Recombinase
Huang, F., Mazina, O. M., Zentner, I., Cocklin, S., & Mazin, A. V. (2012) · Journal of Medicinal Chemistry · doi:10.1021/jm201173g · Cited by 140 · see citing works
Hypoxia as a biomarker for radioresistant cancer stem cells
Peitzsch, C., Perrin, R. L., Hill, R. P., Dubrovska, A., & Kurth, I. (2014) · International Journal of Radiation Biology · doi:10.3109/09553002.2014.916841 · Cited by 142 · see citing works
Prostate-targeted radiosensitization via aptamer-shRNA chimeras in human tumor xenografts
Ni, X., Zhang, Y., Ribas, J., Chowdhury, W. H., Castanares, M. A., Zhang, Z., Laiho, M., DeWeese, T. L., & Lupold, S. E. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45109 · Cited by 139 · see citing works
The role of the DNA damage response in neuronal development, organization and maintenance
Barzilai, A., Biton, S., & Shiloh, Y. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.005 · Cited by 135 · see citing works
Chronic hypoxia compromises repair of DNA double-strand breaks to drive genetic instability
Kumareswaran, R., Ludkovski, O., Meng, A. X., Sykes, J. R., Pintilie, M., & Bristow, R. G. (2012) · Journal of Cell Science · doi:10.1242/jcs.092262 · Cited by 130 · see citing works
Bakr, A., Oing, C., Köcher, S., Borgmann, K., Dornreiter, I., Petersen, C., Dikomey, E., & Mansour, W. Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv160 · Cited by 131 · see citing works
Prognostic and Predictive Role of JWA and XRCC1 Expressions in Gastric Cancer
Wang, S., Wu, X., Chen, Y., Zhang, J., Ding, J., Zhou, Y., He, S., Tan, Y., Qiang, F., Bai, J., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-2863 · Cited by 129 · see citing works
FOXM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance
Khongkow, P., Karunarathna, U., Khongkow, M., Gong, C., Gomes, A., Yagüe, E., Monteiro, L. J., Kongsema, M., Zona, S., Man, E. P. S., et al. (2013) · Oncogene · doi:10.1038/onc.2013.457 · Cited by 127 · see citing works
Yoshimoto, K., Mizoguchi, M., Hata, N., Murata, H., Hatae, R., Amano, T., Nakamizo, A., & Sasaki, T. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00186 · Cited by 126 · see citing works
Jekimovs, C., Bolderson, E., Suraweera, A., Adams, M. N., O'Byrne, K. J., & Richard, D. J. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00086 · Cited by 118 · see citing works
ZEB1 confers chemotherapeutic resistance to breast cancer by activating ATM
Zhang, X., Zhang, Z., Zhang, Q., Zhang, Q., Sun, P., Xiang, R., Ren, G., & Yang, S. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0087-3 · Cited by 123 · see citing works
Prevo, R., Deutsch, É., Sampson, O. L., Diplexcito, J., Cengel, K. A., Harper, J. V., O’Neill, P., McKenna, W. G., Patel, S. K., & Bernhard, E. J. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0757 · Cited by 118 · see citing works
Chan, N. H. L., & Bristow, R. G. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0527 · Cited by 120 · see citing works
Loss of epigenetic silencing in tumors preferentially affects primate-specific retroelements
Szpakowski, S., Sun, X., Lage, J. M., Dyer, A., Rubinstein, J., Kowalski, D., Sasaki, C., Costa, J., & Lizardi, P. M. (2009) · Gene · doi:10.1016/j.gene.2009.08.006 · Cited by 127 · see citing works
CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1
Quennet, V., Beucher, A., Barton, O., Takeda, S., & Löbrich, M. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1175 · Cited by 120 · see citing works
Birch-Machin, M. A., Russell, E. V., & Latimer, J. A. (2013) · British Journal of Dermatology · doi:10.1111/bjd.12207 · Cited by 112 · see citing works
Mao, Z., Jiang, Y., Liu, X., Seluanov, A., & Gorbunova, V. A. (2009) · Neoplasia · doi:10.1593/neo.09312 · Cited by 112 · see citing works
Shirode, A. B., Kovvuru, P., Chittur, S. V., Henning, S. M., Heber, D., & Reliene, R. (2013) · Molecular Carcinogenesis · doi:10.1002/mc.21995 · Cited by 113 · see citing works
Loss of CHD1 causes DNA repair defects and enhances prostate cancer therapeutic responsiveness
Kari, V., Mansour, W. Y., Raul, S. K., Baumgart, S. J., Mund, A., Grade, M., Sirma, H., Simon, R., Will, H., Dobbelstein, M., et al. (2016) · EMBO Reports · doi:10.15252/embr.201642352 · Cited by 111 · see citing works
Xu, B., Hua, J., Zhang, Y., Jiang, X., Zhang, H., Ma, T., Wei, Z., Sun, R., Shen, W. D., Sha, J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016046 · Cited by 110 · see citing works
RAD51 overexpression is a negative prognostic marker for colorectal adenocarcinoma
Tennstedt, P., Fresow, R., Simon, R., Marx, A. H., Terracciano, L., Petersen, C., Sauter, G., Dikomey, E., & Borgmann, K. (2012) · International Journal of Cancer · doi:10.1002/ijc.27907 · Cited by 109 · see citing works
Role of exosomes in malignant glioma: microRNAs and proteins in pathogenesis and diagnosis
Ghaemmaghami, A. B., Mahjoubin‐Tehran, M., Movahedpour, A., Morshedi, K., Sheida, A., Taghavi, S. P., Mirzaei, H., & Hamblin, M. R. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00623-9 · Cited by 107 · see citing works
Effects of phytochemicals on ionization radiation-mediated carcinogenesis and cancer therapy
Nambiar, D. K., Rajamani, P., & Singh, R. P. (2011) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2011.07.005 · Cited by 108 · see citing works
Xu, D., Li, Y., Yin, S., & Huang, F. (2024) · Chemical Society Reviews · doi:10.1039/d3cs00926b · Cited by 108 · see citing works
Roos, W. P., Nikolova, T., Quirós, S., Naumann, S. C., Kiedron, O., Zdzienicka, M. Z., & Kaina, B. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.09.003 · Cited by 106 · see citing works
Choudhury, A., Zhao, H. W., Jalali, F., Rashid, S. A., Ran, J., Supiot, S., Kiltie, A. E., & Bristow, R. G. (2009) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-08-0959 · Cited by 106 · see citing works
Lam, M., Carmichael, A. R., & Griffiths, H. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040152 · Cited by 105 · see citing works
Morita, R., Nakane, S., Shimada, A., Inoue, M., Iino, H., Wakamatsu, T., Fukui, K., Nakagawa, N., Masui, R., & Kuramitsu, S. (2010) · Journal of Nucleic Acids · doi:10.4061/2010/179594 · Cited by 107 · see citing works
DNA Damage and Pulmonary Hypertension
Ranchoux, B., Meloche, J., Paulin, R., Boucherat, O., Provencher, S., & Bonnet, S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060990 · Cited by 105 · see citing works
Persistently bound Ku at DNA ends attenuates DNA end resection and homologous recombination
Shao, Z., Davis, A. J., Fattah, K. R., So, S., Sun, J., Lee, K. J., Harrison, L., Yang, J., & Chen, D. J. (2012) · DNA repair · doi:10.1016/j.dnarep.2011.12.007 · Cited by 103 · see citing works
Targeting BRCA1- and BRCA2-deficient cells with RAD52 small molecule inhibitors
Huang, F., Goyal, N., Sullivan, K., Hanamshet, K., Patel, M., Mazina, O. M., Wang, C. X., An, W. F., Spoonamore, J. E., Metkar, S. R., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw087 · Cited by 100 · see citing works
Receptor signaling as a regulatory mechanism of DNA repair
Meyn, R. E., Munshi, A., Haymach, J. V., Milas, L., & Ang, K. K. (2009) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2009.06.031 · Cited by 101 · see citing works
Chappell, W. H., Gautam, D., Ok, S. T., Johnson, B. A., Anacker, D. C., & Moody, C. A. (2015) · Journal of Virology · doi:10.1128/jvi.02495-15 · Cited by 96 · see citing works
Unboxing the molecular modalities of mutagens in cancer
Kumari, S., Sharma, S., Advani, D., Khosla, A., Kumar, P., & Ambasta, R. K. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-16726-w · Cited by 105 · see citing works
Zheng, L., Dai, H., Zhou, M., Li, X., Liu, C., Guo, Z., Wu, X., Wu, J., Wang, C., Zhong, J., et al. (2012) · Nature Communications · doi:10.1038/ncomms1825 · Cited by 99 · see citing works
The role of RPA2 phosphorylation in homologous recombination in response to replication arrest
Shi, W., Feng, Z., Zhang, J., González-Suárez, I., Vanderwaal, R. P., Wu, X., Powell, S. N., Roti, J. L. R., Gonzalo, S., & Zhang, J. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq035 · Cited by 95 · see citing works
DNA double-strand breaks: Their production, recognition, and repair in eukaryotes
Ohnishi, T., Mori, E., & Takahashi, A. (2009) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2009.06.010 · Cited by 98 · see citing works
Wongsurawat, T., Jenjaroenpun, P., Kwoh, C. K., & Kuznetsov, V. A. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1075 · Cited by 98 · see citing works
Gong, L., Zhang, Y., Zhao, J., Zhang, Y., Tu, K., Jiao, L., Xu, Q., Zhang, M., & Han, S. (2022) · Small · doi:10.1002/smll.202107656 · Cited by 97 · see citing works
Transcription-Associated Recombination Is Dependent on Replication in Mammalian Cells
Gottipati, P., Cassel, T. N., Savolainen, L., & Helleday, T. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00816-07 · Cited by 95 · see citing works
Self-citationAl-Minawi, A. Z., Lee, Y.-F., Hakansson, D., Johansson, F., Lundin, C., Saleh-Gohari, N., Schultz, N. D., Jenssen, D., Bryant, H. E., Meuth, M., et al. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp705 · Cited by 93 · see citing works
Self-citationO’Driscoll, M., & Jeggo, P. A. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.018 · Cited by 92 · see citing works
Attene‐Ramos, M. S., Wagner, E. D., & Plewa, M. J. (2010) · Environmental Science & Technology · doi:10.1021/es1000193 · Cited by 93 · see citing works
From “Cellular” RNA to “Smart” RNA: Multiple Roles of RNA in Genome Stability and Beyond
Michelini, F., Jalihal, A. P., Francia, S., Meers, C., Neeb, Z. T., Rossiello, F., Gioia, U., Aguado, J., Jones-Weinert, C., Luke, B., et al. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00487 · Cited by 85 · see citing works
Opposing roles for 53BP1 during homologous recombination
Kakarougkas, A., Ismail, A., Klement, K., Goodarzi, A. A., Conrad, S., Freire, R., Shibata, A., Löbrich, M., & Jeggo, P. A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt729 · Cited by 87 · see citing works
- Authors
- HELLEDAY, T., LO, J., VANGENT, D., & ENGELWARD, B.
- Affiliations
- Stockholm University (SE)
- Massachusetts Institute of Technology (US)
- Venue
- DNA Repair
- Publisher
- Elsevier BV
- Published
- 2007-07-01
- Volume
- 6
- Issue
- 7
- Pages
- 923-935
- ISSN
- 1568-7856 (ISSN-L)
- 1568-7864
- OpenAlex
- W2077892030
- Cited by
- 640
- References
- 132
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 9 · 2023: 10 · 2022: 22 · 2021: 23 · 2020: 32 · 2019: 29 · 2018: 22 · 2017: 22 · 2016: 36 · 2015: 42 · 2014: 52 · 2013: 60 · 2012: 53
- FWCI
- 19.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- DNA repair (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Keywords
- DNA double-strand break repair, homologous recombination, non-homologous end joining, genome stability, cell cycle checkpoints, apoptosis signaling, premature aging, cancer, targeted cancer therapy
- MeSH terms
- Animals, Cell Cycle, Cell Transformation, Neoplastic, DNA Repair, DNA Replication, Humans, Neoplasms, Recombination, Genetic, Gene Rearrangement, Genomic Instability, DNA Repair Enzymes, DNA Breaks, Double-Stranded
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