Dynamics of DNA Double-Strand Breaks Revealed by Clustering of Damaged Chromosome Domains
Abstract
Interactions between ends from different DNA double-strand breaks (DSBs) can produce tumorigenic chromosome translocations. Two theories for the juxta-position of DSBs in translocations, the static "contact-first" and the dynamic "breakage-first" theory, differ fundamentally in their requirement for DSB mobility. To determine whether or not DSB-containing chromosome domains are mobile and can interact, we introduced linear tracks of DSBs in nuclei. We observed changes in track morphology within minutes after DSB induction, indicating movement of the domains. In a subpopulation of cells, the domains clustered. Juxtaposition of different DSB-containing chromosome domains through clustering, which was most extensive in G1 phase cells, suggests an adhesion process in which we implicate the Mre11 complex. Our results support the breakage-first theory to explain the origin of chromosomal translocations.
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DSBs have the potential to directly affect the 3D genome organization.
“DSBs have the potential to directly affect the 3D genome organization”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [53]
Cites
Megabase Chromatin Domains Involved in DNA Double-Strand Breaks in Vivo
Rogakou, E. P., Boon, C., Redon, C., & Bonner, W. M. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.5.905 · Cited by 2,422 · see citing works
Stewart, G. S., Maser, R. S., Stankovic, T., Bressan, D. A., Kaplan, M. I., Jaspers, N. G. J., Raams, A., Byrd, P. J., Petrini, J. H. J., & Taylor, A. M. R. (1999) · Cell · doi:10.1016/s0092-8674(00)81547-0 · Cited by 1,060 · see citing works
Quantitative Detection of<sup>125</sup>IdU-Induced DNA Double-Strand Breaks with γ-H2AX Antibody
Sedelnikova, O. A., Rogakou, E. P., Panyutin, I. G., & Bonner, W. M. (2002) · Radiation Research · doi:10.1667/0033-7587(2002)158[0486:qdoiid]2.0.co;2 · Cited by 611 · see citing works
Chromatin Motion Is Constrained by Association with Nuclear Compartments in Human Cells
Chubb, J. R., Boyle, S., Perry, P., & Bickmore, W. A. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00695-4 · Cited by 580 · 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
Self-citationIn situ visualization of DNA double-strand break repair in human fibroblasts
Nelms, B. E., Maser, R. S., MacKay, J. F., Lagally, M. G., & Petrini, J. H. J. (1998) · Science · doi:10.1126/science.280.5363.590 · Cited by 500 · see citing works
Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre
Lisby, M., Mortensen, U. H., & Rothstein, R. J. (2003) · Nature Cell Biology · doi:10.1038/ncb997 · Cited by 430 · see citing works
DNA Damage-Dependent Nuclear Dynamics of the Mre11 Complex
Mirzoeva, O. K., & Petrini, J. H. J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.281-288.2001 · Cited by 387 · see citing works
NBS1 Localizes to γ-H2AX Foci through Interaction with the FHA/BRCT Domain
Kobayashi, J., Tauchi, H., Sakamoto, S., Nakamura, A., Morishima, K.-I., Matsuura, S., Kobayashi, T., Tamai, K., Tanimoto, K., & Komatsu, K. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01259-9 · Cited by 306 · see citing works
S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes.
Tashiro, S., Kotomura, N., Shinohara, A., Tanaka, K., Ueda, K., & Kamada, N. (1996) · PubMed · Cited by 165 · see citing works
TYPES AND FREQUENCIES OF CHROMOSOMAL ABERRATIONS INDUCED BY X-RAYSPreprint
Sax, K. (1941) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1941.009.01.012 · Cited by 161 · see citing works
Anderson, R. M., Stevens, D. L., & GOODHEAD, D. T. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182426799 · Cited by 159 · see citing works
Biological Imaging of Heavy Charged-Particle Tracks
Jakob, B., Scholz, M., & Taucher-Scholz, G. (2003) · Radiation Research · doi:10.1667/0033-7587(2003)159[0676:biohct]2.0.co;2 · Cited by 156 · see citing works
Barendsen, G. W. (1962) · Nature · doi:10.1038/1931153a0 · Cited by 150 · see citing works
Human Genome and Diseases:¶Double-strand breaks and translocations in cancer
Elliott, B., & Jasin, M. (2002) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-002-8429-3 · Cited by 144 · see citing works
Dianov, G. L., O’Neill, P., & GOODHEAD, D. T. (2001) · BioEssays · doi:10.1002/bies.1104 · Cited by 110 · see citing works
A General Scheme for the Origin of Mutations
Serebrovsky, A. S. (1929) · The American Naturalist · doi:10.1086/280271 · Cited by 69 · see citing works
Savage, J. R. K. (2000) · Science · doi:10.1126/science.290.5489.62 · Cited by 66 · see citing works
A Model for Interphase Chromosomes and Evaluation of Radiation-Induced Aberrations
Holley, W. R., Mian, S. I., Park, S.-J., Rydberg, B., & Chatterjee, A. (2002) · Radiation Research · doi:10.1667/0033-7587(2002)158[0568:amfica]2.0.co;2 · Cited by 62 · see citing works
Ludwików, G., Xiao, Y., Hoebe, R. A., Franken, N. A. P., Darroudi, F., Stap, J., van Oven, C. H., Noorden, C. J. F. V., & Aten, J. A. (2002) · International Journal of Radiation Biology · doi:10.1080/09553000110110086 · Cited by 23 · see citing works
Self-citationChromosome Organization: Reaching out to Embrace New Models
Wyman, C., & Kanaar, R. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00941-7 · Cited by 18 · see citing works
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Sorted by citations
DNA double-strand break repair-pathway choice in somatic mammalian cells
Scully, R., Panday, A., Elango, R., & Willis, N. A. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0152-0 · Cited by 1,445 · see citing works
Living on a break: cellular senescence as a DNA-damage response
d'Adda di Fagagna, F. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2440 · Cited by 1,170 · see citing works
Choreography of the DNA Damage Response
Lisby, M., Barlow, J. H., Burgess, R. C., & Rothstein, R. (2004) · Cell · doi:10.1016/j.cell.2004.08.015 · Cited by 891 · see citing works
Repair of Strand Breaks by Homologous RecombinationPreprint
Jasin, M., & Rothstein, R. J. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012740 · Cited by 876 · see citing works
DNA Double-Strand Break Repair: All's Well that Ends Well
Wyman, C., & Kanaar, R. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090451 · Cited by 806 · see citing works
Self-citationBranco, M. R., & Pombo, A. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040138 · Cited by 685 · see citing works
Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks
Bekker‐Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M. B., Bártek, J., & Lukas, J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200510130 · Cited by 621 · see citing works
Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks
Kruhlak, M. J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Müller, W. G., McNally, J. G., Bazett-Jones, D. P., & Nussenzweig, A. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200510015 · Cited by 518 · see citing works
Positional stability of single double-strand breaks in mammalian cells
Soutoglou, E., Dorn, J. F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., Danuser, G., & Misteli, T. (2007) · Nature Cell Biology · doi:10.1038/ncb1591 · Cited by 515 · 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
The emerging role of nuclear architecture in DNA repair and genome maintenance
Misteli, T., & Soutoglou, E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2651 · Cited by 468 · see citing works
Phase separation of 53BP1 determines liquid‐like behavior of DNA repair compartments
Kilic, S., Lezaja, A., Gatti, M., Bianco, E., Michelena, J., Imhof, R., & Altmeyer, M. (2019) · The EMBO Journal · doi:10.15252/embj.2018101379 · Cited by 434 · see citing works
Silva, G., Poirot, L., Galetto, R., Smith, J. N. P., Montoya, G., Duchateau, P. N., & Pâques, F. (2011) · Current Gene Therapy · doi:10.2174/156652311794520111 · Cited by 413 · see citing works
Moyal, L., Lerenthal, Y., Gana‐Weisz, M., Mass, G., So, S., Wang, S., Eppink, B., Chung, Y. M., Shalev, G., Shema, E., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.02.015 · Cited by 402 · see citing works
Self-citationNuclear ARP2/3 drives DNA break clustering for homology-directed repair
Schrank, B. R., Aparicio, T., Li, Y., Chang, W., Chait, B. T., Gundersen, G. G., Gottesman, M. E., & Gautier, J. (2018) · Nature · doi:10.1038/s41586-018-0237-5 · Cited by 400 · see citing works
DNA Damage-Dependent Acetylation and Ubiquitination of H2AX Enhances Chromatin Dynamics
Ikura, T., Tashiro, S., Kakino, A., Shima, H., Jacob, N. K., Amunugama, R., Yoder, K. E., Izumi, S., Kuraoka, I., Tanaka, K., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00579-07 · Cited by 376 · see citing works
Interchromosomal Homology Searches Drive Directional ALT Telomere Movement and Synapsis
Cho, N. W., Dilley, R. L., Lampson, M. A., & Greenberg, R. A. (2014) · Cell · doi:10.1016/j.cell.2014.08.030 · Cited by 364 · see citing works
Increased chromosome mobility facilitates homology search during recombination
Miné-Hattab, J., & Rothstein, R. J. (2012) · Nature Cell Biology · doi:10.1038/ncb2472 · Cited by 364 · 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
Dion, V., Kalck, V., Horigome, C., Towbin, B. D., & Gasser, S. M. (2012) · Nature Cell Biology · doi:10.1038/ncb2465 · Cited by 315 · see citing works
Mechanisms that regulate localization of a DNA double-strand break to the nuclear peripheryPreprint
Oza, P., Jaspersen, S. L., Miele, A., Dekker, J., & Peterson, C. L. (2009) · Genes & Development · doi:10.1101/gad.1782209 · Cited by 314 · see citing works
Spatial Dynamics of Chromosome Translocations in Living Cells
Roukos, V., Voss, T. C., Schmidt, C. K., Lee, S., Wangsa, D., & Misteli, T. (2013) · Science · doi:10.1126/science.1237150 · Cited by 312 · see citing works
53BP1 and the LINC Complex Promote Microtubule-Dependent DSB Mobility and DNA Repair
Lottersberger, F., Karssemeijer, R. A., Dimitrova, N., & de Lange, T. (2015) · Cell · doi:10.1016/j.cell.2015.09.057 · Cited by 311 · see citing works
Cellular machineries for chromosomal DNA repairPreprint
Peterson, C. L., & Côté, J. (2004) · Genes & Development · doi:10.1101/gad.1182704 · Cited by 287 · see citing works
DNA Damage Response: Three Levels of DNA Repair Regulation
Sirbu, B. M., & Cortez, D. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012724 · Cited by 272 · see citing works
Saleh-Gohari, N. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh703 · Cited by 270 · see citing works
Evidence for formation of DNA repair centers and dose-response nonlinearity in human cells
Neumaier, T., Swenson, J., Pham, C., Polyzos, A. A., Lo, A. T., Yang, P., Dyball, J., Asaithamby, A., Chen, D. J., Bissell, M. J., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117849108 · Cited by 266 · see citing works
Heterochromatin protein 1 is recruited to various types of DNA damage
Luijsterburg, M. S., Dinant, C., Lans, H., Stap, J., Wiernasz, E., Lagerwerf, S., Warmerdam, D. O., Lindh, M., Brink, M. C., Dobrucki, J. W., et al. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200810035 · Cited by 264 · see citing works
Self-citationAymard, F., Aguirrebengoa, M., Guillou, E., Javierre, B. M., Bugler, B., Arnould, C., Rocher, V., Iacovoni, J. S., Biernacka, A., Skrzypczak, M., et al. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3387 · Cited by 263 · see citing works
RAD51 Gene Family Structure and Function
Bonilla, B., Hengel, S. R., Grundy, M. K., & Bernstein, K. A. (2020) · Annual Review of Genetics · doi:10.1146/annurev-genet-021920-092410 · Cited by 259 · see citing works
Targeted chromosomal deletions in human cells using zinc finger nucleasesPreprint
Lee, H. J., Kim, E., & Kim, J. (2009) · Genome Research · doi:10.1101/gr.099747.109 · Cited by 250 · 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
McManus, K. J., & Hendzel, M. J. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-01-0065 · Cited by 242 · see citing works
Two-step activation of ATM by DNA and the Mre11–Rad50–Nbs1 complex
Dupré, A., Boyer-Châtenet, L., & Gautier, J. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1090 · Cited by 233 · see citing works
53BP1: a DSB escortPreprint
Mirman, Z., & de Lange, T. (2020) · Genes & Development · doi:10.1101/gad.333237.119 · Cited by 231 · 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
Kao, G. D., Jiang, Z., Fernandes, A. M., Gupta, A., & Maity, A. M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703042200 · Cited by 225 · see citing works
Chromatin Movement in the Maintenance of Genome Stability
Dion, V., & Gasser, S. M. (2013) · Cell · doi:10.1016/j.cell.2013.02.010 · Cited by 223 · see citing works
Therizols, P., Fairhead, C., Cabal, G. G., Genovesio, A., Olivo‐Marín, J., Dujon, B., & Fabre, E. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200505159 · Cited by 217 · see citing works
Puizina, J., Široký, J., Mokroš, P., Schweizer, D., & Říha, K. (2004) · The Plant Cell · doi:10.1105/tpc.104.022749 · Cited by 213 · see citing works
Spatial genome organization in the formation of chromosomal translocations
Meaburn, K. J., Misteli, T., & Soutoglou, E. (2006) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2006.10.008 · Cited by 212 · see citing works
Wuerffel, R., Wang, L., Grigera, F., Manis, J. P., Selsing, E., Perlot, T., Alt, F. W., Cogné, M., Pinaud, E., & Kenter, A. L. (2007) · Immunity · doi:10.1016/j.immuni.2007.09.007 · Cited by 208 · see citing works
Costes, S. V., Chiolo, I., Pluth, J. M., Barcellos‐Hoff, M. H., & Jakob, B. (2010) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.006 · Cited by 204 · see citing works
Homologous recombination-mediated double-strand break repair
Wyman, C., Ristić, D., & Kanaar, R. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.03.037 · Cited by 195 · see citing works
Self-citationMin, J., Wright, W. E., & Shay, J. W. (2017) · Molecular and Cellular Biology · doi:10.1128/mcb.00226-17 · Cited by 194 · see citing works
Live cell microscopy analysis of radiation-induced DNA double-strand break motion
Jakob, B., Splinter, J., Durante, M., & Taucher-Scholz, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810987106 · Cited by 191 · see citing works
Induction and quantification of γ-H2AX foci following low and high LET-irradiation
Leatherbarrow, E. L., Harper, J. V., Cucinotta, F. A., & O’Neill, P. (2006) · International Journal of Radiation Biology · doi:10.1080/09553000600599783 · Cited by 189 · see citing works
ATM Prevents the Persistence and Propagation of Chromosome Breaks in Lymphocytes
Callén, E., Janković, M., Difilippantonio, S., Daniel, J. A., Chen, H. T., Celeste, A., Pellegrini, M., McBride, K. M., Wangsa, D., Bredemeyer, A. L., et al. (2007) · Cell · doi:10.1016/j.cell.2007.06.016 · Cited by 178 · see citing works
Chromatin compartmentalization regulates the response to DNA damage
Arnould, C., Rocher, V., Saur, F., Bader, A. S., Muzzopappa, F., Collins, S., Lesage, E., Bozec, B. L., Puget, N., Clouaire, T., et al. (2023) · Nature · doi:10.1038/s41586-023-06635-y · Cited by 177 · see citing works
Plo, I., Nakatake, M., Malivert, L., de Villartay, J., Giraudier, S., Villeval, J., Wiesmüller, L., & Vainchenker, W. (2008) · Blood · doi:10.1182/blood-2008-01-134114 · Cited by 176 · see citing works
Aprataxin, a novel protein that protects against genotoxic stress
Gueven, N. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh122 · Cited by 175 · see citing works
Markova, E. N., Schultz, N. D., & Belyaev, I. Y. (2007) · International Journal of Radiation Biology · doi:10.1080/09553000601170469 · Cited by 173 · see citing works
R-loops as Janus-faced modulators of DNA repair
Marnef, A., & Legube, G. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00663-4 · Cited by 170 · see citing works
Misteli, T. (2004) · Cell · doi:10.1016/j.cell.2004.09.035 · Cited by 169 · see citing works
Weinstock, D. M., Richardson, C. A., Elliott, B., & Jasin, M. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.028 · Cited by 168 · see citing works
The biogenesis of chromosome translocations
Roukos, V., & Misteli, T. (2014) · Nature Cell Biology · doi:10.1038/ncb2941 · Cited by 166 · 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
Mechanisms that Promote and Suppress Chromosomal Translocations in Lymphocytes
Gostissa, M., Alt, F. W., & Chiarle, R. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101329 · Cited by 156 · see citing works
Costes, S. V., Boissière, A., Ravani, S. A., Romano, R., Parvin, B., & Barcellos‐Hoff, M. H. (2006) · Radiation Research · doi:10.1667/rr3538.1 · Cited by 153 · see citing works
Chromatin mobility is increased at sites of DNA double-strand breaks
Krawczyk, P. M., Borovski, T., Stap, J., Cijsouw, T., ten Cate, R., Medema, J. P., Kanaar, R., Franken, N. A. P., & Aten, J. A. (2012) · Journal of Cell Science · doi:10.1242/jcs.089847 · Cited by 152 · see citing works
Self-citationRadioprotection of <i>IDH1</i> -Mutated Cancer Cells by the IDH1-Mutant Inhibitor AGI-5198
Molenaar, R. J., Botman, D., Smits, M. A., Hira, V. V., van Lith, S. A., Stap, J., Henneman, P., Khurshed, M., Lenting, K., Mul, A. N., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3603 · Cited by 148 · see citing works
Self-citationDNA damage checkpoint and repair centers
Lisby, M., & Rothstein, R. J. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.03.011 · Cited by 148 · see citing works
RAD-ical New Insights into RAD51 Regulation
Sullivan, M. R., & Bernstein, K. A. (2018) · Genes · doi:10.3390/genes9120629 · Cited by 144 · see citing works
The time and spatial effects of bystander response in mammalian cells induced by low dose radiation
Hu, B., Wu, L., Han, W., Zhang, L., Chen, S., Xu, A., Hei, T. K., & Yu, Z. (2005) · Carcinogenesis · doi:10.1093/carcin/bgi224 · Cited by 142 · see citing works
Nuclear actin filaments in DNA repair dynamics
Caridi, C. P., Plessner, M., Grosse, R., & Chiolo, I. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0379-1 · Cited by 127 · see citing works
Chromatin dynamics during DSB repair
Falk, M., Lukášová, E., Gabrielova, B., Ondřej, V., & Kozubek, S. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.07.002 · Cited by 135 · see citing works
Carcinogenic lead chromate induces DNA double-strand breaks in human lung cells
Xie, H., Wise, S. S., Holmes, A. L., Xu, B., Wakeman, T. P., Pelsue, S. C., Singh, N. P., & Wise, J. P. (2005) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2005.06.002 · Cited by 132 · see citing works
Higher-order chromatin structure in DSB induction, repair and misrepair
Falk, M., Lukášová, E., & Kozubek, S. (2010) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2010.01.013 · Cited by 131 · see citing works
Engreitz, J., Agarwala, V., & Mirny, L. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044196 · Cited by 131 · see citing works
Dileep, V., Boix, C. A., Mathys, H., Marco, A., Welch, G. M., Meharena, H. S., Loon, A., Jeloka, R., Peng, Z., Bennett, D. A., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.038 · Cited by 130 · see citing works
Uranium Induces Apoptosis and Is Genotoxic to Normal Rat Kidney (NRK-52E) Proximal Cells
Thiebault, C., Carrière, M., Milgram, S., Simon-Deckers, A., Avoscan, L., & Gouget, B. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm130 · Cited by 130 · see citing works
Principles of chromosomal organization: lessons from yeast
Zimmer, C., & Fabre, E. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201010058 · Cited by 127 · see citing works
Chromothripsis in cancer cells: An update
Rode, A., Maaß, K. K., Willmund, K. V., Lichter, P., & Ernst, A. (2015) · International Journal of Cancer · doi:10.1002/ijc.29888 · Cited by 125 · see citing works
Non-redundant Functions of ATM and DNA-PKcs in Response to DNA Double-Strand Breaks
Caron, P., Choudjaye, J., Clouaire, T., Bugler, B., Daburon, V., Aguirrebengoa, M., Mangeat, T., Iacovoni, J. S., Álvarez-Quilón, A., Cortés‐Ledesma, F., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.10.024 · Cited by 124 · see citing works
Sridharan, D. M., Asaithamby, A., Bailey, S. M., Costes, S. V., Doetsch, P. W., Dynan, W. S., Kronenberg, A., Rithidech, K. N., Saha, J., Snijders, A. M., et al. (2015) · Radiation Research · doi:10.1667/rr13804.1 · Cited by 124 · see citing works
Replication Stress in Mammalian Cells and Its Consequences for Mitosis
Gelot, C., Magdalou, I., & López, B. S. (2015) · Genes · doi:10.3390/genes6020267 · Cited by 123 · see citing works
H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy
Bewersdorf, J., Bennett, B. T., & Knight, K. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608709103 · Cited by 121 · see citing works
Choreography of recombination proteins during the DNA damage response
Lisby, M., & Rothstein, R. J. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.007 · Cited by 118 · see citing works
Belyaev, I. Y. (2010) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2010.01.011 · Cited by 117 · see citing works
Use of γH2AX and Other Biomarkers of Double-Strand Breaks During Radiotherapy
Sak, A., & Stuschke, M. (2010) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2010.05.004 · Cited by 113 · see citing works
Dealing with DNA damage: Relationships between checkpoint and repair pathways
Warmerdam, D. O., & Kanaar, R. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.001 · Cited by 113 · see citing works
Self-citationImmunofluorescence Detection of Clustered γ-H2AX Foci Induced by HZE-Particle Radiation
Desai, N., Davis, E. J., O'Neill, P., Durante, M., Cucinotta, F. A., & Wu, H. (2005) · Radiation Research · doi:10.1667/rr3431.1 · Cited by 111 · see citing works
Mre11 Assembles Linear DNA Fragments into DNA Damage Signaling Complexes
Costanzo, V., Paull, T., Gottesman, M., & Gautier, J. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020110 · Cited by 106 · see citing works
Mobility and immobility of chromatin in transcription and genome stability
Soutoglou, E., & Misteli, T. (2007) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2007.08.004 · Cited by 106 · see citing works
Amitai, A., Seeber, A., Gasser, S. M., & Holcman, D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.018 · Cited by 103 · see citing works
Image-Based Modeling Reveals Dynamic Redistribution of DNA Damage into Nuclear Sub-Domains
Costes, S. V., Ponomarev, A. L., Chen, J. L., Nguyen, D. H. A., Cucinotta, F. A., & Barcellos‐Hoff, M. H. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030155 · Cited by 103 · see citing works
Mathas, S., Kreher, S., Meaburn, K. J., Jöhrens, K., Lamprecht, B., Assaf, C., Sterry, W., Kadin, M. E., Daibata, M., Joos, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900912106 · Cited by 102 · see citing works
Replication Stress Induces Micronuclei Comprising of Aggregated DNA Double-Strand Breaks
Xu, B., Sun, Z.-L., Liu, Z., Guo, H., Liu, Q., Jiang, H., Zou, Y., Gong, Y., Tischfield, J. A., & Shao, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018618 · Cited by 101 · see citing works
Comparison of High- and Low-LET Radiation-Induced DNA Double-Strand Break Processing in Living Cells
Roobol, S. J., van den Bent, I., van Cappellen, W. A., Abraham, T. E., Paul, M. W., Kanaar, R., Houtsmuller, A. B., van Gent, D. C., & Essers, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186602 · Cited by 98 · see citing works
Self-citationPerinuclear tethers license telomeric DSBs for a broad kinesin- and NPC-dependent DNA repair process
Chung, D. K. C., Chan, J. N. Y., Strecker, J. G., Zhang, W., Ebrahimi‐Ardebili, S., Lu, T., Abraham, K. J., Durocher, D., & Mekhail, K. (2015) · Nature Communications · doi:10.1038/ncomms8742 · Cited by 98 · see citing works
Antibody Class Switching Mediated by Yeast Endonuclease-Generated DNA Breaks
Zarrin, A. A., Fitz, C. D. V., Tseng, E., Gleason, M., Zarin, P., Tian, M., & Alt, F. W. (2006) · Science · doi:10.1126/science.1136386 · Cited by 98 · see citing works
Lukas, C., Bártek, J., & Lukas, J. (2005) · Chromosoma · doi:10.1007/s00412-005-0011-y · Cited by 97 · see citing works
Hyperthermia-induced DNA repair deficiency suggests novel therapeutic anti-cancer strategies
Eppink, B., Krawczyk, P. M., Stap, J., & Kanaar, R. (2012) · International Journal of Hyperthermia · doi:10.3109/02656736.2012.695427 · Cited by 96 · see citing works
Self-citationFunctional Nuclear Architecture Studied by Microscopy
Rouquette, J., Cremer, C. G., Cremer, T. J., & Fakan, S. (2010) · International review of cytology · doi:10.1016/s1937-6448(10)82001-5 · Cited by 95 · see citing works
Franken, N. A. P., ten Cate, R., Krawczyk, P. M., Stap, J., HAVEMAN, J., Aten, J. A., & Barendsen, G. W. (2011) · Radiation Oncology · doi:10.1186/1748-717x-6-64 · Cited by 94 · see citing works
Self-citationFunctional Taxonomy of Bacterial Hyperstructures
Norris, V., den Blaauwen, T., Cabin‐Flaman, A., Doi, R. H., Harshey, R. M., Jannière, L., Jiménez‐Sánchez, A., Jin, D. J., Levin, P. A., Mileykovskaya, E., et al. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00035-06 · Cited by 94 · see citing works
Antonelli, F., Campa, A., Esposito, G., Giardullo, P., Belli, M., Dini, V., Meschini, S., Simone, G., Sorrentino, E., Gerardi, S., et al. (2015) · Radiation Research · doi:10.1667/rr13855.1 · Cited by 92 · see citing works
Parada, L. A. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.03.013 · Cited by 89 · see citing works
Oshidari, R., Strecker, J. G., Chung, D. K. C., Abraham, K. J., Chan, J. N. Y., Damaren, C. J., & Mekhail, K. (2018) · Nature Communications · doi:10.1038/s41467-018-05009-7 · Cited by 88 · see citing works
Han, W., Wu, L., Chen, S., Bao, L., Zhang, L., Jiang, E., Zhao, Y., Xu, A., Hei, T. K., & Zhang, Y. (2006) · Oncogene · doi:10.1038/sj.onc.1210024 · Cited by 88 · see citing works
- Authors
- Aten, J. A., Stap, J., Krawczyk, P. M., van Oven, C. H., Hoebe, R. A., Essers, J., & Kanaar, R.
- Affiliations
- Erasmus MC (NL)
- Center for Microscopical Research, Department of Cell Biology and Histology, Academic Medical Center, University of Amsterdam, P.O. Box 22700, 1100 DE Amsterdam, Netherlands.
- Corresponding author
- Kanaar, Roland
- Venue
- Science
- Published
- 2004-01-02
- Volume
- 303
- Issue
- 5654
- Pages
- 92-95
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2041251646
- Cited by
- 491
- References
- 21
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 11 · 2023: 18 · 2022: 12 · 2021: 23 · 2020: 18 · 2019: 17 · 2018: 26 · 2017: 26 · 2016: 16 · 2015: 17 · 2014: 22 · 2013: 26 · 2012: 24
- FWCI
- 13.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Keywords
- DNA double-strand breaks, chromosomal translocation, Mre11 complex, G1 phase, carcinogenesis
- MeSH terms
- MRE11 Homologue Protein, Alpha Particles, Animals, Ataxia Telangiectasia, Cell Nucleus, Chromosomes, Human, Cricetulus, DNA, DNA Damage, DNA Repair, DNA-Binding Proteins, Fibroblasts, Cricetinae, HeLa Cells, Histones, Humans, Phosphorylation, Translocation, Genetic, G1 Phase, G2 Phase, S Phase, CHO Cells, Chromosome Breakage, Chromosomes, Mammalian, Rad51 Recombinase
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