More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance

Glioma stem cells promote radioresistance by preferential activation of the DNA damage response

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DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139

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The DNA Damage Response: Making It Safe to Play with Knives

Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368

Inhibition of Poly(ADP-Ribose) Polymerase in Tumors from BRCA Mutation Carriers

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ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage

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53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks

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A guide to super-resolution fluorescence microscopy

Schermelleh, L., Heintzmann, R., & Leonhardt, H. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201002018 · Cited by 1,258

Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications

Polo, S. E., & Jackson, S. P. (2011) · Genes & Development · doi:10.1101/gad.2021311 · Cited by 1,092

Systematic Protein Location Mapping Reveals Five Principal Chromatin Types in Drosophila Cells

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Structural Basis for the Methylation State-Specific Recognition of Histone H4-K20 by 53BP1 and Crb2 in DNA Repair

Botuyan, M. V., Lee, J., Ward, I. M., Kim, J., Thompson, J. R., Chen, J., & Mer, G. (2006) · Cell · doi:10.1016/j.cell.2006.10.043 · Cited by 1,011

53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers

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RNF168 Binds and Amplifies Ubiquitin Conjugates on Damaged Chromosomes to Allow Accumulation of Repair Proteins

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Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks

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The PARP Side of the Nucleus: Molecular Actions, Physiological Outcomes, and Clinical Targets

Krishnakumar, R., & Kraus, W. L. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.06.017 · Cited by 877

The RIDDLE Syndrome Protein Mediates a Ubiquitin-Dependent Signaling Cascade at Sites of DNA Damage

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ATM-Dependent Chromatin Changes Silence Transcription In cis to DNA Double-Strand Breaks

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Chromatin Challenges during DNA Replication and Repair

Groth, A., Rocha, W., Verreault, A., & Almouzni, G. (2007) · Cell · doi:10.1016/j.cell.2007.01.030 · Cited by 733

53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress

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Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining

Miller, K. M., Tjeertes, J. V., Coates, J., Legube, G., Polo, S. E., Britton, S., & Jackson, S. P. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1899 · Cited by 629

Replication stress induces sister-chromatid bridging at fragile site loci in mitosis

Chan, K., Palmai‐Pallag, T., Ying, S., & Hickson, I. D. (2009) · Nature Cell Biology · doi:10.1038/ncb1882 · Cited by 601

Poly(ADP-ribose)–Dependent Regulation of DNA Repair by the Chromatin Remodeling Enzyme ALC1

Ahel, D., Hořejší, Z., Wiechens, N., Polo, S. E., Garcia-Wilson, E., Ahel, I., Flynn, H., Skehel, M., West, S. C., Jackson, S. P., et al. (2009) · Science · doi:10.1126/science.1177321 · Cited by 588

CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle

Yun, M. H., & Hiom, K. (2009) · Nature · doi:10.1038/nature07955 · Cited by 556

Double-Strand Breaks in Heterochromatin Move Outside of a Dynamic HP1a Domain to Complete Recombinational Repair

Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A. A., Costes, S. V., & Karpen, G. H. (2011) · Cell · doi:10.1016/j.cell.2011.02.012 · Cited by 547

Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks

Galanty, Y., Belotserkovskaya, R., Coates, J., Polo, S. E., Miller, K. M., & Jackson, S. P. (2009) · Nature · doi:10.1038/nature08657 · Cited by 536

Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions

Cook, P. J., Ju, B. G., Telese, F., Wang, X., Glass, C. K., & Rosenfeld, M. G. (2009) · Nature · doi:10.1038/nature07849 · Cited by 534

A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage

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High‐resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome

Iacovoni, J. S., Caron, P., Lassadi, I., Nicolas, E., Massip, L., Trouche, D., & Legube, G. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.38 · Cited by 515

Positional stability of single double-strand breaks in mammalian cells

Soutoglou, E., Dorn, J. F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., Danuser, G., & Misteli, T. (2007) · Nature Cell Biology · doi:10.1038/ncb1591 · Cited by 509

Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair

Berkovich, E., Monnat, R. J., & Kastan, M. B. (2007) · Nature Cell Biology · doi:10.1038/ncb1599 · Cited by 477

Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60

Sun, Y., Jiang, X., Xu, Y., Ayrapetov, M. K., Moreau, L. A., Whetstine, J. R., & Price, B. D. (2009) · Nature Cell Biology · doi:10.1038/ncb1982 · Cited by 454

Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction

Fierz, B., Chatterjee, C., McGinty, R. K., Bar‐Dagan, M., Raleigh, D. P., & Muir, T. W. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.501 · Cited by 435

WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity

Xiao, A., Li, H., Shechter, D., Ahn, S. H., Fabrizio, L. A., Erdjument‐Bromage, H., Ishibe-Murakami, S., Wang, B., Tempst, P., Hofmann, K., et al. (2008) · Nature · doi:10.1038/nature07668 · Cited by 430

Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins

Ahel, I., Ahel, D., Matsusaka, T., Clark, A. J., Pines, J., Boulton, S. J., & West, S. C. (2008) · Nature · doi:10.1038/nature06420 · Cited by 429

MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites

Pei, H., Zhang, L. M., Luo, K., Qin, Y., Chesi, M., Fei, Y. F., Bergsagel, P. L., Wang, L., You, Z., & Lou, Z. (2011) · Nature · doi:10.1038/nature09658 · Cited by 425

HP1-β mobilization promotes chromatin changes that initiate the DNA damage response

Ayoub, N., Jeyasekharan, A. D. D., Bernal, J. A., & Venkitaraman, A. R. (2008) · Nature · doi:10.1038/nature06875 · Cited by 417

Requirement of ATM-Dependent Monoubiquitylation of Histone H2B for Timely Repair of DNA Double-Strand Breaks

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 416

Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site

Letessier, A., Millot, G. A., Koundrioukoff, S., Lachagès, A.-M., Vogt, N., Hansen, R. S., Malfoy, B., Brison, O., & Debatisse, M. (2011) · Nature · doi:10.1038/nature09745 · Cited by 414

DNA Damage-Dependent Acetylation and Ubiquitination of H2AX Enhances Chromatin Dynamics

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Double Strand Breaks Can Initiate Gene Silencing and SIRT1-Dependent Onset of DNA Methylation in an Exogenous Promoter CpG Island

O'Hagan, H. M., Mohammad, H. P., & Baylin, S. B. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000155 · Cited by 386

The Smc5–Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus

Torres‐Rosell, J., Šunjevarić, I., Piccoli, G. D., Sacher, M., Eckert‐Boulet, N., Reid, R. J. D., Jentsch, S., Rothstein, R. J., Aragón, L., & Lisby, M. (2007) · Nature Cell Biology · doi:10.1038/ncb1619 · Cited by 379

The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress

Morris, J. R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., Butler, L., Galanty, Y., Pangon, L., Kiuchi, T., et al. (2009) · Nature · doi:10.1038/nature08593 · Cited by 375

Regulation of DNA‐damage responses and cell‐cycle progression by the chromatin remodelling factor CHD4

Polo, S. E., Kaidi, A., Baskcomb, L., Galanty, Y., & Jackson, S. P. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.188 · Cited by 374 · cited 1×

Regulation of Homologous Recombination by RNF20-Dependent H2B Ubiquitination

Nakamura, K., Kato, A., Kobayashi, J., Yanagihara, H., Sakamoto, S., Oliveira, D. V. N. P., Shimada, M., Tauchi, H., Suzuki, H., Tashiro, S., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.02.002 · Cited by 361

Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler

Gottschalk, A. J., Timinszky, G., Kong, S. E., Jin, J., Cai, Y., Swanson, S. K., Washburn, M. P., Florens, L. A., Ladurner, A. G., Conaway, J. W., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906920106 · Cited by 358

Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1

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Replication stress induces 53BP1-containing OPT domains in G1 cells

Harrigan, J. A., Belotserkovskaya, R., Coates, J., Dimitrova, D. S., Polo, S. E., Bradshaw, C. R., Fraser, P., & Jackson, S. P. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201011083 · Cited by 357

PARP-3 and APLF Function Together to Accelerate Nonhomologous End-Joining

Rulten, S. L., Fisher, A. E. O., Robert, I., Zuma, M. C., Rouleau, M., Ju, L., Poirier, G. G., Reina‐San‐Martin, B., & Caldecott, K. W. (2011) · Molecular Cell · doi:10.1016/j.molcel.2010.12.006 · Cited by 355

A Selective Requirement for 53BP1 in the Biological Response to Genomic Instability Induced by Brca1 Deficiency

Cao, L., Xu, X., Bunting, S. F., Liu, J., Wang, R.-H., Cao, L. L., Wu, J. J., Peng, T.-N., Chen, J., Nussenzweig, A., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.06.037 · Cited by 324

53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination

Bothmer, A., Robbiani, D. F., Feldhahn, N., Gazumyan, A., Nussenzweig, A., & Nussenzweig, M. C. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20100244 · Cited by 315

RAD18 transmits DNA damage signalling to elicit homologous recombination repair

Huang, J., Huen, M. S. Y., Kim, H., Leung, C. C. Y., Glover, J. N. M., Yu, X., & Chen, J. (2009) · Nature Cell Biology · doi:10.1038/ncb1865 · Cited by 308

The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax

Goodarzi, A. A., Jeggo, P., & Lobrich, M. (2010) · DNA Repair · doi:10.1016/j.dnarep.2010.09.013 · Cited by 305

Epigenetic Instability due to Defective Replication of Structured DNA

Sarkies, P., Reams, C., Simpson, L. J., & Sale, J. E. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.11.009 · Cited by 302

Replication Stress Interferes with Histone Recycling and Predeposition Marking of New Histones

Jasencakova, Z., Scharf, A. N. D., Ask, K., Corpet, A., Imhof, A., Almouzni, G., & Groth, A. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.033 · Cited by 279

HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes

Bekker‐Jensen, S., Danielsen, J. M. R., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bártek, J., Lukas, J., & Mailand, N. (2009) · Nature Cell Biology · doi:10.1038/ncb2008 · Cited by 277

Heterochromatin is refractory to γ-H2AX modification in yeast and mammals

Kim, J., Kruhlak, M. J., Dotiwala, F., Nussenzweig, A., & Haber, J. E. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200612031 · Cited by 276

PARP1 ADP-ribosylates lysine residues of the core histone tails

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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

DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2APreprint

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BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair

Ismail, I. H., Andrin, C., McDonald, D., & Hendzel, M. J. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201003034 · Cited by 255

KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response

Goodarzi, A. A., Kurka, T., & Jeggo, P. A. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2077 · Cited by 255

Regulation of the Histone H4 Monomethylase PR-Set7 by CRL4Cdt2-Mediated PCNA-Dependent Degradation during DNA Damage

Oda, H., Hübner, M. R., Beck, D. B., Vermeulen, M., Hurwitz, J., Spector, D. L., & Reinberg, D. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.011 · Cited by 253

BMI1 Confers Radioresistance to Normal and Cancerous Neural Stem Cells through Recruitment of the DNA Damage Response Machinery

Facchino, S., Abdouh, M., Chatoo, W., & Bernier, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1634-10.2010 · Cited by 253

The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage

Larsen, D. H., Poinsignon, C., Guðjόnsson, Þ., Dinant, C., Payne, M., Hari, F. J., Danielsen, J. M. R., Ménard, P., Sand, J. C., Stucki, M., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200912135 · Cited by 251

Regulation of DNA End Joining, Resection, and Immunoglobulin Class Switch Recombination by 53BP1

Bothmer, A., Robbiani, D. F., Di Virgilio, M., Bunting, S. F., Klein, I. A., Feldhahn, N., Barlow, J., Chen, H.-T., Bosque, D., Callen, E., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.03.019 · Cited by 244

RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear fociPreprint

Hu, Y., Scully, R., Sobhian, B., Xie, A., Shestakova, E. A., & Livingston, D. M. (2011) · Genes & Development · doi:10.1101/gad.2011011 · Cited by 244

The NuRD chromatin–remodeling complex regulates signaling and repair of DNA damage

Smeenk, G., Wiegant, W. W., Vrolijk, H., Solari, A. P., Pastink, A., & van Attikum, H. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201001048 · Cited by 243

Global chromatin compaction limits the strength of the DNA damage response

Murga, M., Jaco, I., Fan, Y., Soria, R., Martínez-Pastor, B., Cuadrado, M., Yang, S.-M., Blasco, M. A., Skoultchi, A. I., & Fernández-Capetillo, Ó. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200704140 · Cited by 236

The BRCA1-RAP80 Complex Regulates DNA Repair Mechanism Utilization by Restricting End Resection

Coleman, K. A., & Greenberg, R. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.213728 · Cited by 234

The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks

Shao, G., Lilli, D. R., Patterson-Fortin, J., Coleman, K. A., Morrissey, D. E., & Greenberg, R. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807485106 · Cited by 221

ATM damage response and XLF repair factor are functionally redundant in joining DNA breaks

Zha, S., Guo, C., Boboilă, C., Oksenych, V., Cheng, H.-L., Zhang, Y., Wesemann, D. R., Yuen, G. J., Patel, H., Goff, P. H., et al. (2010) · Nature · doi:10.1038/nature09604 · Cited by 209

Formation of Dynamic γ-H2AX Domains along Broken DNA Strands Is Distinctly Regulated by ATM and MDC1 and Dependent upon H2AX Densities in Chromatin

Savic, V., Yin, B., Maas, N. L., Bredemeyer, A. L., Carpenter, A. C., Helmink, B. A., Yang-Iott, K. S., Sleckman, B. P., & Bassing, C. H. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.04.012 · Cited by 204

HP1α recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair

Baldeyron, C., Soria, G., Roche, D., Cook, A. J. L., & Almouzni, G. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201101030 · Cited by 200

MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cellsPreprint

Ichijima, Y., Ichijima, M., Lou, Z., Nussenzweig, A., Camerini‐Otero, R. D., Chen, J., Andreassen, P. R., & Namekawa, S. H. (2011) · Genes & Development · doi:10.1101/gad.2030811 · Cited by 200

Histone methyltransferase Dot1 and Rad9 inhibit single‐stranded DNA accumulation at DSBs and uncapped telomeres

Lazzaro, F., Sapountzi, V., Granata, M., Pellicioli, A., Vaze, M. B., Haber, J. E., Plevani, P., Lydall, D. A., & Muzi-Falconi, M. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.81 · Cited by 198

The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair

Xu, Y., Sun, Y., Jiang, X., Ayrapetov, M. K., Moskwa, P., Yang, S., Weinstock, D. M., & Price, B. D. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201001160 · Cited by 194

BRIT1/MCPH1 links chromatin remodelling to DNA damage response

Peng, G., Yim, E.-K., Dai, H., Jackson, A. P., van der Burgt, I., Pan, M., Hu, R., Li, K., & Lin, S. (2009) · Nature Cell Biology · doi:10.1038/ncb1895 · Cited by 191

A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses

Lilley, C. E., Chaurushiya, M. S., Boutell, C., Landry, S., Suh, J., Panier, S., Everett, R. D., Stewart, G. S., Durocher, D., & Weitzman, M. D. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.400 · Cited by 181

Chromatin dynamics and the repair of DNA double strand breaks

Xu, Y., & Price, B. D. (2011) · Cell Cycle · doi:10.4161/cc.10.2.14543 · Cited by 172

BBAP Monoubiquitylates Histone H4 at Lysine 91 and Selectively Modulates the DNA Damage Response

Yan, Q., Dutt, S., Xu, R., Graves, K., Juszczyński, P., Manis, J. P., & Shipp, M. A. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.08.019 · Cited by 171

DNA Repair Factor APLF Is a Histone Chaperone

Mehrotra, P. V., Ahel, D., Ryan, D., Weston, R., Wiechens, N., Kraehenbuehl, R., Owen‐Hughes, T., & Ahel, I. (2011) · Molecular Cell · doi:10.1016/j.molcel.2010.12.008 · Cited by 161

APLF (C2orf13) Is a Novel Human Protein Involved in the Cellular Response to Chromosomal DNA Strand Breaks

Iles, N., Rulten, S. L., El‐Khamisy, S. F., & Caldecott, K. W. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02269-06 · Cited by 159

A novel human AP endonuclease with conserved zinc‐finger‐like motifs involved in DNA strand break responses

Kanno, S., Kuzuoka, H., Sasao, S., Hong, Z., Lan, L., Nakajima, S., & Yasui, A. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601663 · Cited by 153

Histone Ubiquitination Associates with BRCA1-Dependent DNA Damage Response

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H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes

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