Regulation of DNA double-strand break repair pathway choice

Shrivastav, Meena; De Haro, Leyma P; Nickoloff, Jac A

doi:10.1038/cr.2007.111

Cited by 1,329DNA Repair MechanismsPARP inhibition in cancer therapyEffects of Radiation Exposure

Regulation of DNA double-strand break repair pathway choice

Shrivastav, Meena, De Haro, Leyma P, Nickoloff, Jac A·2008·Cell Research

DOI 10.1038/cr.2007.111

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Abstract

DNA double-strand breaks (DSBs) are critical lesions that can result in cell death or a wide variety of genetic alterations including large- or small-scale deletions, loss of heterozygosity, translocations, and chromosome loss. DSBs are repaired by non-homologous end-joining (NHEJ) and homologous recombination (HR), and defects in these pathways cause genome instability and promote tumorigenesis. DSBs arise from endogenous sources including reactive oxygen species generated during cellular metabolism, collapsed replication forks, and nucleases, and from exogenous sources including ionizing radiation and chemicals that directly or indirectly damage DNA and are commonly used in cancer therapy. The DSB repair pathways appear to compete for DSBs, but the balance between them differs widely among species, between different cell types of a single species, and during different cell cycle phases of a single cell type. Here we review the regulatory factors that regulate DSB repair by NHEJ and HR in yeast and higher eukaryotes. These factors include regulated expression and phosphorylation of repair proteins, chromatin modulation of repair factor accessibility, and the availability of homologous repair templates. While most DSB repair proteins appear to function exclusively in NHEJ or HR, a number of proteins influence both pathways, including the MRE11/RAD50/NBS1(XRS2) complex, BRCA1, histone H2AX, PARP-1, RAD18, DNA-dependent protein kinase catalytic subunit (DNA-PKcs), and ATM. DNA-PKcs plays a role in mammalian NHEJ, but it also influences HR through a complex regulatory network that may involve crosstalk with ATM, and the regulation of at least 12 proteins involved in HR that are phosphorylated by DNA-PKcs and/or ATM.

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Homologous recombination uses a long homologous sequence in S/G2 when sister chromatids are templates.
“Homologous recombination uses a long homologous sequence to guide repair in the S phase and G2 phase of the cell cycle, in which sister chromatids are available as templates125.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [125]

Capturing Chromosome Conformation
Dekker, J., Rippe, K., Dekker, M., & Kleckner, N. (2002) · Science · doi:10.1126/science.1067799 · Cited by 3,652 · see citing works
Multiple Pathways of Recombination Induced by Double-Strand Breaks in <i>Saccharomyces cerevisiae</i>
Pâques, F., & Haber, J. E. (1999) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.63.2.349-404.1999 · Cited by 2,120 · see citing works
ATM Phosphorylates Histone H2AX in Response to DNA Double-strand Breaks
Burma, S., Chen, B. P., Murphy, M., Kurimasa, A., & Chen, D. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100466200 · Cited by 1,954 · see citing works
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 · see citing works
Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM
Hickson, I., Zhao, Y., Richardson, C. J., Green, S. J., Martin, N. M. B., Orr, A. I., Reaper, P. M., Jackson, S. P., Curtin, N. J., & Smith, G. C. M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-2727 · Cited by 1,220 · see citing works
Molecular views of recombination proteins and their control
West, S. C. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1127 · Cited by 947 · see citing works
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 · see citing works
PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways
Wang, M., Wu, W., Wu, W., Rosidi, B., Zhang, L., Wang, H., & Iliakis, G. E. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl840 · Cited by 823 · see citing works
Recombination Proteins in Yeast
Krogh, B. O., & Symington, L. S. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.091500 · Cited by 804 · see citing works
Saccharomyces Ku70, Mre11/Rad50, and RPA Proteins Regulate Adaptation to G2/M Arrest after DNA Damage
Lee, S. E., Moore, J. K., Holmes, A. M., Umezu, K., Kolodner, R. D., & Haber, J. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81482-8 · Cited by 775 · see citing works
Cell Cycle and Genetic Requirements of Two Pathways of Nonhomologous End-Joining Repair of Double-Strand Breaks in Saccharomyces cerevisiae
Moore, J. K., & Haber, J. E. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.5.2164 · Cited by 728 · 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
BRCA2 Function in DNA Binding and Recombination from a BRCA2-DSS1-ssDNA Structure
Yang, H., Jeffrey, P. D., Miller, J. J., Kinnucan, E., Sun, Y., Thomä, N. H., Zheng, N., Chen, P., Lee, W., & Pavletich, N. P. (2002) · Science · doi:10.1126/science.297.5588.1837 · Cited by 705 · see citing works
Interfaces Between the Detection, Signaling, and Repair of DNA Damage
Rouse, J. W., & Jackson, S. P. (2002) · Science · doi:10.1126/science.1074740 · Cited by 688 · see citing works
A role for Saccharomyces cerevisiae histone H2A in DNA repair
Downs, J. A., Lowndes, N. F., & Jackson, S. P. (2000) · Nature · doi:10.1038/35050000 · Cited by 650 · see citing works
Stable Interaction between the Products of the BRCA1 and BRCA2 Tumor Suppressor Genes in Mitotic and Meiotic Cells
Chen, J., Silver, D. P., Walpita, D., Cantor, S. B., Gazdar, A. F., Tomlinson, G. E., Couch, F. J., Weber, B. L., Ashley, T., Livingston, D. M., et al. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80276-2 · Cited by 635 · see citing works
The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability
Gudmundsdottir, K. K., & Ashworth, A. (2006) · Oncogene · doi:10.1038/sj.onc.1209874 · Cited by 625 · see citing works
Chromosome territories – a functional nuclear landscape
Cremer, T., Cremer, M., Dietzel, S., Müller, S., Solovei, I. V., & Fakan, S. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.04.007 · Cited by 601 · see citing works
MECHANISM AND CONTROL OF V(D)J RECOMBINATION AT THE IMMUNOGLOBULIN HEAVY CHAIN LOCUS
Jung, D., Giallourakis, C. C., Mostoslavsky, R., & Alt, F. W. (2006) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115830 · Cited by 578 · see citing works
Role of the human RAD51 protein in homologous recombination and double-stranded-break repair
Baumann, P., & West, S. C. (1998) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(98)01232-8 · Cited by 570 · see citing works
Partners and pathways
Haber, J. E. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02022-9 · Cited by 564 · see citing works
Differential usage of non-homologous end-joining and homologous recombination in double strand break repair
Sonoda, E., Hochegger, H., Saberi, A., Taniguchi, Y., & Takeda, S. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.022 · Cited by 527 · see citing works
Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae.
Kadyk, L. C., & Hartwell, L. H. (1992) · Genetics · doi:10.1093/genetics/132.2.387 · Cited by 522 · see citing works
Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cellsPreprint
Pierce, A. J., Hu, P., Han, M., Ellis, N. A., & Jasin, M. (2001) · Genes & Development · doi:10.1101/gad.946401 · Cited by 514 · see citing works
Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaksPreprint
Chan, D. W., Chen, B. P.-C., Prithivirajsingh, S., Kurimasa, A., Story, M. D., Qin, J., & Chen, D. J. (2002) · Genes & Development · doi:10.1101/gad.1015202 · Cited by 479 · see citing works
CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair
Esashi, F., Christ, N., Gannon, J., Liu, Y., Hunt, T., Jasin, M., & West, S. C. (2005) · Nature · doi:10.1038/nature03404 · Cited by 473 · see citing works
The Nuclease Activity of Mre11 Is Required for Meiosis but Not for Mating Type Switching, End Joining, or Telomere Maintenance
Moreau, S., Ferguson, J. R., & Symington, L. S. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.1.556 · Cited by 445 · see citing works
ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage
Aladjem, M. I., Spike, B. T., Rodewald, L. W., Hope, T. J., Klemm, M., Jaenisch, R., & Wahl, G. M. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70061-2 · Cited by 442 · see citing works
Disruption of Mouse RAD54 Reduces Ionizing Radiation Resistance and Homologous Recombination
Essers, J., Hendriks, R. W., Swagemakers, S. M. A., Troelstra, C., de Wit, J., Bootsma, D., Hoeijmakers, J. H. J., & Kanaar, R. (1997) · Cell · doi:10.1016/s0092-8674(00)80199-3 · Cited by 435 · see citing works
ATM stabilizes DNA double-strand-break complexes during V(D)J recombination
Bredemeyer, A. L., Sharma, G. G., Huang, C., Helmink, B. A., Walker, L. M., Khor, K. C., Nuskey, B., Sullivan, K. E., Pandita, T. K., Bassing, C. H., et al. (2006) · Nature · doi:10.1038/nature04866 · Cited by 425 · see citing works
Role of non-homologous end joining (NHEJ) in maintaining genomic integrity
Burma, S., Chen, B. P. C., & Chen, D. J. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.026 · Cited by 423 · see citing works
The life and death of DNA-PK
Collis, S. J., DeWeese, T. L., Jeggo, P. A., & Parker, A. R. (2004) · Oncogene · doi:10.1038/sj.onc.1208332 · Cited by 417 · see citing works
γH2AX and MDC1: Anchoring the DNA-damage-response machinery to broken chromosomes
Stucki, M., & Jackson, S. P. (2006) · DNA Repair · doi:10.1016/j.dnarep.2006.01.012 · Cited by 412 · see citing works
Nonhomologous End Joining in Yeast
Daley, J. M., Palmbos, P. L., Wu, D. L., & Wilson, T. E. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.113340 · Cited by 408 · see citing works
The Many Interfaces of Mre11
Haber, J. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81626-8 · Cited by 407 · 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
Characterization of Double-Strand Break-Induced Recombination: Homology Requirements and Single-Stranded DNA Formation
Sugawara, N., & Haber, J. E. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.2.563-575.1992 · Cited by 378 · see citing works
Repair of DNA double strand breaks by non-homologous end joining
Lees‐Miller, S. P. (2003) · Biochimie · doi:10.1016/j.biochi.2003.10.011 · Cited by 367 · see citing works
The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations
Ferguson, D. O., Sekiguchi, J., Chang, S. S., Frank, K. M., Gao, Y., DePinho, R. A., & Alt, F. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.110152897 · Cited by 356 · see citing works
A Double-Strand Break Repair Defect in ATM-Deficient Cells Contributes to Radiosensitivity
Kühne, M., Riballo, E., Rief, N., Rothkamm, K., Jeggo, P. A., & Löbrich, M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2384 · Cited by 347 · see citing works
Replication‐mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA‐dependent protein kinase and dissociates RPA:DNA‐PK complexes
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
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 · see citing works
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 · see citing works
Cell Cycle Dependence of DNA-dependent Protein Kinase Phosphorylation in Response to DNA Double Strand Breaks
Chen, B. P. C., Chan, D. W., Kobayashi, J., Burma, S., Asaithamby, A., Morotomi‐Yano, K., Botvinick, E. L., Qin, J., & Chen, D. J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408827200 · Cited by 320 · see citing works
Replication fork pausing and recombination or “gimme a break”Preprint
Rothstein, R. J., Michel, B., & Gangloff, S. (2000) · Genes & Development · doi:10.1101/gad.14.1.1 · Cited by 320 · see citing works
SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination
Myung, K., Datta, A., Chen, C., & Kolodner, R. D. (2001) · Nature Genetics · doi:10.1038/83673 · Cited by 316 · see citing works
The controlling role of ATM in homologous recombinational repair of DNA damage
Morrison, C., Sonoda, E., Takao, N., Shinohara, A., Yamamoto, K., & Takeda, S. (2000) · The EMBO Journal · doi:10.1093/emboj/19.3.463 · Cited by 312 · see citing works
Requirement for the Kinase Activity of Human DNA-Dependent Protein Kinase Catalytic Subunit in DNA Strand Break Rejoining
Kurimasa, A., Kumano, S., Boubnov, N. V., Story, M. D., Tung, C., Peterson, S., & Chen, D. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3877 · Cited by 298 · see citing works
Ataxia Telangiectasia Mutated (ATM) Is Essential for DNA-PKcs Phosphorylations at the Thr-2609 Cluster upon DNA Double Strand Break
Chen, B. P. C., Uematsu, N., Kobayashi, J., Lerenthal, Y., Krempler, A., Yajima, H., Löbrich, M., Shiloh, Y., & Chen, D. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m611605200 · Cited by 296 · see citing works
Cellular functions of the BRCA tumour-suppressor proteins
Boulton, S. J. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340633 · Cited by 292 · see citing works
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 · see citing works
Chromatin dynamics and the preservation of genetic information
Downs, J. A., Nussenzweig, M. C., & Nussenzweig, A. (2007) · Nature · doi:10.1038/nature05980 · Cited by 285 · see citing works
DNA synthesis errors associated with double-strand-break repair.
Strathern, J. N., Shafer, B. K., & McGill, C. B. (1995) · Genetics · doi:10.1093/genetics/140.3.965 · Cited by 282 · see citing works
Direct DNA binding by Brca1
Paull, T. T., Cortez, D., Bowers, B., Elledge, S. J., & Gellert, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111125998 · Cited by 282 · see citing works
Mutations in Two Ku Homologs Define a DNA End-Joining Repair Pathway in Saccharomyces cerevisiae
Milne, G. T., Jin, S., Shannon, K. B., & Weaver, D. T. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4189 · Cited by 278 · see citing works
Reduced X-Ray Resistance and Homologous Recombination Frequencies in a RAD54 Mutant of the Chicken DT40 Cell Line
Bezzubova, O. Y., Silbergleit, A., Yamaguchi‐Iwai, Y., Takeda, S., & Buerstedde, J.-M. (1997) · Cell · doi:10.1016/s0092-8674(00)80198-1 · Cited by 277 · see citing works
Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2
Esashi, F., Galkin, V. E., Yu, X., Egelman, E. H., & West, S. C. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1245 · Cited by 277 · see citing works
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 · see citing works
Regulation of DNA repair by ubiquitylation
Huang, T. T., & D’Andrea, A. D. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1908 · Cited by 273 · see citing works
The Mre11-Rad50-Xrs2 Protein Complex Facilitates Homologous Recombination-Based Double-Strand Break Repair in Saccharomyces cerevisiae
Bressan, D. A., Baxter, B. K., & Petrini, J. H. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.11.7681 · Cited by 271 · see citing works
Evolution of the Immunoglobulin Heavy Chain Class Switch Recombination Mechanism
Chaudhuri, J., Basu, U., Zarrin, A. A., Yan, C. T., Franco, S., Perlot, T., Vuong, B. Q., Wang, J. H., Phan, R. T., Datta, A., et al. (2007) · Advances in immunology · doi:10.1016/s0065-2776(06)94006-1 · Cited by 263 · 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
p53 in recombination and repair
Gatz, S. A., & Wiesmüller, L. (2006) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401903 · Cited by 242 · see citing works
Mutations in XRS2 and RAD50 Delay but Do Not Prevent Mating-Type Switching in Saccharomyces cerevisiae
Ivanov, E. L., Sugawara, N., White, C. I., Fabre, F., & Haber, J. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.5.3414-3425.1994 · Cited by 240 · see citing works
High Spontaneous Intrachromosomal Recombination Rates in Ataxia-Telangiectasia
Meyn, M. S. (1993) · Science · doi:10.1126/science.8493577 · Cited by 237 · see citing works
Different Roles for Nonhomologous End Joining and Homologous Recombination following Replication Arrest in Mammalian Cells
Lundin, C., Erixon, K., Arnaudeau, C., Schultz, N., Jenssen, D., Meuth, M., & Helleday, T. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.16.5869-5878.2002 · Cited by 234 · see citing works
NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae
Valencia‐Burton, M., Bentele, M., Vaze, M. B., Herrmann, G., Kraus, E., Lee, S. E., Schär, P., & Haber, J. E. (2001) · Nature · doi:10.1038/414666a · Cited by 228 · see citing works
Cellular Responses to DNA Damage: One Signal, Multiple Choices
Su, T. T. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090428 · Cited by 227 · see citing works
Inactivation of p53 results in high rates of homologous recombination
Mekeel, K. L., Tang, W., Kachnic, L. A., Luo, C., DeFrank, J. S., & Powell, S. N. (1997) · Oncogene · doi:10.1038/sj.onc.1201143 · Cited by 223 · see citing works
Evidence for DNA-PK-Dependent and -Independent DNA Double-Strand Break Repair Pathways in Mammalian Cells as a Function of the Cell Cycle
Lee, S. E., Mitchell, R. A., Cheng, A., & Hendrickson, E. A. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.3.1425 · Cited by 222 · see citing works
Surveillance of Different Recombination Defects in Mouse Spermatocytes Yields Distinct Responses despite Elimination at an Identical Developmental Stage
Barchi, M., Mahadevaiah, S. K., Giacomo, M. D., Baudat, F., de Rooij, D. G., Burgoyne, P. S., Jasin, M., & Keeney, S. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7203-7215.2005 · Cited by 222 · see citing works
Werner Syndrome Protein Is Regulated and Phosphorylated by DNA-dependent Protein Kinase
Yannone, S. M., Roy, S., Chan, D. W., Murphy, M. B., Huang, S., Campisi, J., & Chen, D. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101913200 · Cited by 221 · see citing works
Role of DNA–PK in the cellular response to DNA double-strand breaks
Burma, S., & Chen, D. J. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.03.021 · Cited by 220 · see citing works
BRCA1, BRCA2, and Rad51 operate in a common DNA damage response pathway.
Chen, J. J., Silver, D. P., Cantor, S., Livingston, D. M., & Scully, R. (1999) · PubMed · Cited by 217 · see citing works
Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation
Keeney, S., & Neale, M. J. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340523 · Cited by 217 · see citing works
UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, γ-H2AX formation, and Mre11 relocalization
Limoli, C. L., Giedzinski, E., Bonner, W. M., & Cleaver, J. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231611798 · Cited by 210 · see citing works
A YY1–INO80 complex regulates genomic stability through homologous recombination–based repair
Wu, S., Shi, Y. G., Mulligan, P., Gay, F., Landry, J. W., Liu, H., Lu, J., Qi, H. H., Wang, W., Nickoloff, J. A., et al. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1332 · Cited by 208 · see citing works
Self-citation
Control of Sister Chromatid Recombination by Histone H2AX
Xie, A., Puget, N., Shim, I., Odate, S., Jarzyna, I., Bassing, C. H., Alt, F. W., & Scully, R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.12.007 · Cited by 208 · see citing works
Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events.
Kramer, K. M., Brock, J., Bloom, K., Moore, J. K., & Haber, J. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.2.1293 · Cited by 205 · see citing works
Radiobiological and Genetic Studies on a Polyploid Series (Haploid to Hexaploid) of Saccharomyces cerevisiae
Mortimer, R. (1958) · Radiation Research · doi:10.2307/3570795 · Cited by 198 · see citing works
Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase
DOUGLAS, P., Sapkota, G. P., MORRICE, N. A., Yu, Y., Goodarzi, A. A., Merkle, D., Meek, K., Alessi, D. R., & Lees‐Miller, S. P. (2002) · Biochemical Journal · doi:10.1042/bj20020973 · Cited by 196 · see citing works
Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths
Lee, S. E., Pâques, F., Sylvan, J. B., & Haber, J. E. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80339-x · Cited by 195 · see citing works
Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation.
Sugawara, N., & Haber, J. E. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.2.563 · Cited by 193 · see citing works
Genetic Requirements for RAD51- andRAD54-Independent Break-Induced Replication Repair of a Chromosomal Double-Strand Break
Signon, L., Malkova, A., Naylor, M. L., Klein, H. L., & Haber, J. E. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.6.2048-2056.2001 · Cited by 185 · 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
Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development
Orii, K. E., Lee, Y., Kondo, N., & McKinnon, P. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602436103 · Cited by 181 · see citing works
DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination
Allen, C., Kurimasa, A., Brenneman, M. A., Chen, D. J., & Nickoloff, J. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052545899 · Cited by 181 · see citing works
Self-citation
DNA Substrate Dependence of p53-Mediated Regulation of Double-Strand Break Repair
Akyüz, N., Boehden, G. S., Süße, S., Rimek, A., Preuß, U., Scheidtmann, K., & Wiesmüller, L. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.17.6306-6317.2002 · Cited by 175 · see citing works
Telomeres and chromosome instability
Murnane, J. P. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.030 · Cited by 174 · see citing works
Mouse RAD54 Affects DNA Double-Strand Break Repair and Sister Chromatid Exchange
Dronkert, M. L. G., Beverloo, H. B., Johnson, R. D., Hoeijmakers, J. H. J., Jasin, M., & Kanaar, R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.9.3147-3156.2000 · Cited by 174 · see citing works
Impaired Nonhomologous End-Joining Provokes Soft Tissue Sarcomas Harboring Chromosomal Translocations, Amplifications, and Deletions
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
The Fission Yeast Taz1 Protein Protects Chromosomes from Ku-Dependent End-to-End Fusions
Ferreira, M. G., & Cooper, J. P. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00154-x · Cited by 173 · see citing works
Interactive competition between homologous recombination and non-homologous end joining.
Allen, C., Halbrook, J., & Nickoloff, J. A. (2003) · PubMed · Cited by 171 · see citing works
Self-citation
Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast
Kegel, A., Sjöstrand, J. O. O., & Åström, S. U. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00488-2 · Cited by 158 · see citing works
Roles of the Bloom's syndrome helicase in the maintenance of genome stability
Cheok, C. F., Bachrati, C. Z., Chan, K., Ralf, C., Wu, L., & Hickson, I. D. (2005) · Biochemical Society Transactions · doi:10.1042/bst20051456 · Cited by 158 · see citing works
Werner Protein Is a Target of DNA-dependent Protein Kinase in Vivo and in Vitro, and Its Catalytic Activities Are Regulated by Phosphorylation
Karmakar, P., Piotrowski, J., Brosh, R. M., Sommers, J. A., Lees‐Miller, S. P., Cheng, W.-H., Snowden, C. M., Ramsden, D. A., & Bohr, V. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111523200 · Cited by 157 · see citing works
Cdc2–cyclin B kinase activity links Crb2 and Rqh1–topoisomerase IIIPreprint
Caspari, T., Murray, J. M., & Carr, A. M. (2002) · Genes & Development · doi:10.1101/gad.221402 · Cited by 156 · see citing works
The DNA-Dependent Protein Kinase Interacts with DNA To Form a Protein−DNA Complex That Is Disrupted by Phosphorylation
Merkle, D., Douglas, P., Moorhead, G. B. G., Leonenko, Z., Yu, Y., Cramb, D. T., Bazett‐Jones, D. P., & Lees‐Miller, S. P. (2002) · Biochemistry · doi:10.1021/bi0263558 · Cited by 155 · see citing works
Protein Phosphatases Regulate DNA-dependent Protein Kinase Activity
Douglas, P., Moorhead, G. B. G., Ye, R., & Lees‐Miller, S. P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011703200 · Cited by 153 · see citing works
Relative rates of homologous and nonhomologous recombination in transfected DNA.
Roth, D. B., & Wilson, J. H. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.10.3355 · Cited by 151 · see citing works
An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells
Delacôte, F. (2002) · Nucleic Acids Research · doi:10.1093/nar/gkf452 · Cited by 148 · see citing works
A DNA Microarray-Based Genetic Screen for Nonhomologous End-Joining Mutants in Saccharomyces cerevisiae
Ooi, S. L., Shoemaker, D. D., & Boeke, J. D. (2001) · Science · doi:10.1126/science.1065672 · Cited by 145 · see citing works
ATP-dependent chromatin remodeling factors and DNA damage repair
Osley, M. A., Tsukuda, T., & Nickoloff, J. A. (2007) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.07.011 · Cited by 141 · see citing works
Self-citation
DNA-Dependent Protein Kinase Phosphorylation Sites in Ku 70/80 Heterodimer
Chan, D. W., Ye, R., Veillette, C., & Lees‐Miller, S. P. (1999) · Biochemistry · doi:10.1021/bi982584b · Cited by 140 · see citing works
Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends
Block, W. D. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh761 · Cited by 139 · see citing works
The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts
Karanjawala, Z. E., Grawunder, U., Hsieh, C., & Lieber, M. R. (1999) · Current Biology · doi:10.1016/s0960-9822(00)80123-2 · Cited by 137 · see citing works
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 · see citing works
Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52
Chen, F., Nastasi, A. J., Shen, Z., Brenneman, M. A., Crissman, H. A., & Chen, D. J. (1997) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(97)00020-7 · Cited by 131 · see citing works
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 · see citing works
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 · see citing works
Yeast cell-type regulation of DNA repair
Åström, S. U., Okamura, S. M., & Rine, J. (1999) · Nature · doi:10.1038/16833 · Cited by 119 · see citing works
Defective DNA repair and increased genomic instability in Cernunnos-XLF-deficient murine ES cells
Zha, S., Alt, F. W., Cheng, H.-L., Brush, J. W., & Li, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611734104 · Cited by 117 · see citing works
Checkpoint Kinase 2–Mediated Phosphorylation of BRCA1 Regulates the Fidelity of Nonhomologous End-Joining
Zhuang, J., Zhang, J., Willers, H., Wang, H., Chung, J. H., van Gent, D. C., Hallahan, D. E., Powell, S. N., & Xia, F. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3278 · Cited by 116 · see citing works
Reverse genetic studies of the DNA damage response in the chicken B lymphocyte line DT40.
Yamazoe, M., Sonoda, E., Hochegger, H., & Takeda, S. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.039 · Cited by 116 · see citing works
Cohesin and DNA damage repair
Watrin, E., & Peters, J. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.06.024 · Cited by 114 · see citing works
Synergistic role of Ku80 and poly(ADP-ribose) polymerase in suppressing chromosomal aberrations and liver cancer formation.
Tong, W., Cortes, U., Hande, M. P., Ohgaki, H., Cavalli, L. R., Lansdorp, P. M., Haddad, B. R., & Wang, Z. (2002) · PubMed · Cited by 113 · see citing works
Activation of DNA-dependent Protein Kinase by Single-stranded DNA Ends
Hammarsten, O., DeFazio, L. G., & Chu, G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.3.1541 · Cited by 109 · see citing works
The DNA-dependent Protein Kinase Catalytic Activity Regulates DNA End Processing by Means of Ku Entry into DNA
Calsou, P., Frit, P., Humbert, O., Muller, C., Chen, D. J., & Salles, B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.12.7848 · Cited by 108 · see citing works
The interaction of p53 with replication protein A mediates suppression of homologous recombination
Romanova, L. Y., Willers, H., Blagosklonny, M. V., & Powell, S. N. (2004) · Oncogene · doi:10.1038/sj.onc.1207982 · Cited by 105 · see citing works
Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control
Willers, H., McCarthy, E. E., Wu, B., Wunsch, H., Tang, W., Taghian, D. G., Xia, F., & Powell, S. N. (2000) · Oncogene · doi:10.1038/sj.onc.1203142 · Cited by 104 · see citing works
RB signaling prevents replication-dependent DNA double-strand breaks following genotoxic insult
Bosco, E. E. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkg919 · Cited by 97 · see citing works
Deficiency in the Catalytic Subunit of DNA-Dependent Protein Kinase Causes Down-Regulation of ATM
Peng, Y., Woods, R. G., Beamish, H., Ye, R., Lees‐Miller, S. P., Lavin, M. F., & Bedford, J. S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3451 · Cited by 95 · see citing works
Pathways that suppress programmed DNA breaks from progressing to chromosomal breaks and translocations
Franco, S., Alt, F. W., & Manis, J. P. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.024 · Cited by 94 · see citing works
Multiple Pathways for Repair of DNA Double-Strand Breaks in Mammalian Chromosomes
Lin, Y., Lukácsovich, T., & Waldman, A. S. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.12.8353 · Cited by 90 · 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
Homologous Recombinational Repair of Double-Strand Breaks in Yeast Is Enhanced by MAT Heterozygosity Through yKU-Dependent and -Independent Mechanisms
Clikeman, J. A., Khalsa, G. J., Barton, S. L., & Nickoloff, J. A. (2001) · Genetics · doi:10.1093/genetics/157.2.579 · Cited by 81 · see citing works
Self-citation
Good Timing in the Cell Cycle for Precise DNA Repair by BRCA1
Durant, S. T., & Nickoloff, J. A. (2005) · Cell Cycle · doi:10.4161/cc.4.9.2027 · Cited by 77 · see citing works
Self-citation
High Frequency and Error-prone DNA Recombination in Ataxia Telangiectasia Cell Lines
Luo, C., Tang, W., Mekeel, K. L., DeFrank, J. S., Anné, P. R., & Powell, S. N. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.8.4497 · Cited by 77 · see citing works
RAD18 and Poly(ADP-Ribose) Polymerase Independently Suppress the Access of Nonhomologous End Joining to Double-Strand Breaks and Facilitate Homologous Recombination-Mediated Repair
Saberi, A., Hochegger, H., Szüts, D., Lan, L., Yasui, A., Sale, J. E., Taniguchi, Y., Murakawa, Y., Zeng, W., Yokomori, K., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01243-06 · Cited by 77 · see citing works
p53 Inhibits Strand Exchange and Replication Fork Regression Promoted by Human Rad51
Yoon, D. J., Wang, Y., Stapleford, K. A., Wiesmüller, L., & Chen, J. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.12.050 · Cited by 75 · see citing works
Inhibition of homologous recombination by variants of the catalytic subunit of the DNA-dependent protein kinase (DNA-PKcs)
Convery, E., Shin, E. K., Ding, Q., Wang, W., Douglas, P., Davis, L. S., Nickoloff, J. A., Lees‐Miller, S. P., & Meek, K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406466102 · Cited by 74 · see citing works
Self-citation
Nature of Lesions Formed by Ionizing Radiation
Ward, J. F. (1998) · Humana Press eBooks · doi:10.1007/978-1-59259-455-9_5 · Cited by 70 · see citing works
DNA repair pathways involved in anaphase bridge formation
Açılan, C., Potter, D. M., & Saunders, W. S. (2007) · Genes Chromosomes and Cancer · doi:10.1002/gcc.20425 · Cited by 66 · see citing works
Diverse Roles for Histone H2A Modifications in DNA Damage Response Pathways in Yeast
Moore, J. D., Yazgan, O., Ataian, Y., & Krebs, J. E. (2006) · Genetics · doi:10.1534/genetics.106.063792 · Cited by 60 · see citing works
Homologous recombination repair is regulated by domains at the N- and C-terminus of NBS1 and is dissociated with ATM functions
Sakamoto, S., Iijima, K., Mochizuki, D., Nakamura, K., Teshigawara, K., Kobayashi, J., Matsuura, S., Tauchi, H., & Komatsu, K. (2007) · Oncogene · doi:10.1038/sj.onc.1210428 · Cited by 58 · see citing works
Playing for half the deck: the molecular biology of meiosis
Champion, M. D., & Hawley, R. S. (2002) · Nature Cell Biology · doi:10.1038/ncb-nm-fertilitys50 · Cited by 56 · see citing works
The Greek Goddess, Artemis, reveals the secrets of her cleavage
Jeggo, P. A. (2002) · DNA repair · doi:10.1016/s1568-7864(02)00096-4 · Cited by 55 · see citing works
GETTING STARTED: Regulating the Initiation of DNA Replication in Yeast
Toone, W. M., Aerne, B. L., Morgan, B. A., & Johnston, A. L. H. (1997) · Annual Review of Microbiology · doi:10.1146/annurev.micro.51.1.125 · Cited by 54 · see citing works
γH2AX as a Checkpoint Maintenance Signal
Downey, M., & Durocher, D. (2006) · Cell Cycle · doi:10.4161/cc.5.13.2899 · Cited by 51 · see citing works
Caffeine inhibits homology-directed repair of I-SceI-induced DNA double-strand breaks
Wang, H., Boecker, W., Wang, H., Wang, X., Guan, J., Thompson, L. H., Nickoloff, J. A., & Iliakis, G. E. (2004) · Oncogene · doi:10.1038/sj.onc.1207168 · Cited by 50 · see citing works
Self-citation
Chromosomal Aberrations and Genomic Instability Induced by Topoisomerase- Targeted Antitumour Drugs
Degrassi, F., Fiore, M., & Palitti, F. (2004) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1568011043352920 · Cited by 43 · see citing works
Different Mating-Type-Regulated Genes Affect the DNA Repair Defects of SaccharomycesRAD51,RAD52andRAD55Mutants
Valencia‐Burton, M., Oki, M., Johnson, J., Seier, T., Kamakaka, R. T., & Haber, J. E. (2006) · Genetics · doi:10.1534/genetics.106.058685 · Cited by 38 · see citing works
Mre11 and Ku regulation of double-strand break repair by gene conversion and break-induced replication
Krishna, S., Wagener, B. M., Liu, H. P., Lo, Y., Sterk, R. T., Petrini, J. H. J., & Nickoloff, J. A. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.01.006 · Cited by 31 · see citing works
Self-citation
Recombination: Mechanisms and Roles in Tumorigenesis
Nickoloff, J. A. (2002) · Elsevier eBooks · doi:10.1016/b0-12-227555-1/00201-x · Cited by 25 · see citing works
Self-citation
Down‐regulation of PARP‐1, but not of Ku80 or DNA‐PKcs, results in higher gene targeting efficiency
Domínguez‐Bendala, J., Masutani, M., & McWhir, J. (2006) · Cell Biology International · doi:10.1016/j.cellbi.2005.12.005 · Cited by 18 · see citing works
Mammalian Homologous Recombination Repair and Cancer Intervention
Shen, Z., & Nickoloff, J. A. (2007) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789812706782_0005 · Cited by 15 · see citing works
Self-citation
BRCA1 and BRCA2 in DNA Repair and Genome Stability
Brenneman, M. A. (2001) · Humana Press eBooks · doi:10.1007/978-1-59259-095-7_10 · Cited by 10 · see citing works
Mating-Type Control of DNA Repair and Recombination in Saccharomyces cerevisiae
Nickoloff, J. A., & Haber, J. E. (2001) · Humana Press eBooks · doi:10.1007/978-1-59259-095-7_5 · Cited by 9 · see citing works
Self-citation
Mating-Type Control of DNA Repair and Recombination in Saccharomyces cerevisiae
Nickoloff, J. A., & Haber, J. E. (2003) · Humana Press eBooks · doi:10.1385/1-59259-095-0:107 · Cited by 4 · see citing works
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The DNA Damage Response: Making It Safe to Play with Knives
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“Conversely, specific types of damage repair can only occur during specific cell cycle phases: the double-strand break homologous repair pathway requires the presence of a sister chromatid‒ a condition only met during the S and G2 phases [6,7].”
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Authors: Shrivastav, M., De Haro, L. P., & Nickoloff, J. A.
Affiliations: University of New Mexico (US)
Corresponding author: Nickoloff, Jac A
ORCID: Nickoloff, Jac A
Venue: Cell Research
Publisher: Springer Science and Business Media LLC
Published: 2007-12-24
Volume: 18
Issue: 1
Pages: 134-147
ISSN: 1001-0602 (ISSN-L)
1748-7838
DOI: 10.1038/cr.2007.111
OpenAlex: W2010711320
Cited by: 1,329
References: 149
Citations by year: 2026: 25 · 2025: 46 · 2024: 54 · 2023: 59 · 2022: 80 · 2021: 80 · 2020: 56 · 2019: 57 · 2018: 70 · 2017: 76 · 2016: 79 · 2015: 79 · 2014: 67 · 2013: 86 · 2012: 83
FWCI: 5.79
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Cell Research (publishedVersion)
PubMed (publishedVersion)
Funders: Michigan State University
College of Engineering, Michigan State University
National Cancer Institute (R01CA100862)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Keywords: DNA double-strand break repair, non-homologous end joining, homologous recombination, DNA-PKcs, ATM, Mre11-Rad50-Nbs1 complex, BRCA1, histone H2AX, PARP1, RAD18, protein phosphorylation, chromatin regulation, genomic instability, DNA damage response
MeSH terms: Animals, Cell Cycle, Chromosome Aberrations, DNA Repair, DNA-Binding Proteins, Eukaryotic Cells, Humans, Models, Biological, Nuclear Proteins, Recombination, Genetic, Species Specificity, Yeasts, Signal Transduction, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Tumor Suppressor Proteins, Genomic Instability, DNA-Activated Protein Kinase, DNA Breaks, Double-Stranded, Ataxia Telangiectasia Mutated Proteins

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Regulation of DNA double-strand break repair pathway choice

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