The emerging role of nuclear architecture in DNA repair and genome maintenance (original) (raw)

• Wyman, C. & Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363–383 (2006).
  CAS PubMed Google Scholar
• Lobrich, M. & Jeggo, P. A. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nature Rev. Cancer 7, 861–869 (2007).
  Google Scholar
• Kanaar, R., Wyman, C. & Rothstein, R. Quality control of DNA break metabolism: in the 'end', it's a good thing. EMBO J. 27, 581–588 (2008).
  CAS PubMed PubMed Central Google Scholar
• Lukas, J., Lukas, C. & Bartek, J. Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Repair 3, 997–1007 (2004).
  CAS PubMed Google Scholar
• Misteli, T. Beyond the sequence: cellular organization of genome function. Cell 128, 787–800 (2007).
  CAS PubMed Google Scholar
• Berkovich, E., Monnat, R. J. Jr & Kastan, M. B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nature Cell Biol. 9, 683–690 (2007).
  CAS PubMed Google Scholar
• Paull, T. T. & Lee, J. H. The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle 4, 737–740 (2005).
  CAS PubMed Google Scholar
• Petrini, J. H. & Stracker, T. H. The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol. 13, 458–462 (2003).
  CAS PubMed Google Scholar
• Costanzo, V., Paull, T., Gottesman, M. & Gautier, J. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2, E110 (2004).
  PubMed PubMed Central Google Scholar
• Lee, J. H. & Paull, T. T. ATM activation by DNA double-strand breaks through the Mre11–Rad50–Nbs1 complex. Science 308, 551–554 (2005).
  CAS PubMed Google Scholar
• Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213–1226 (2005).
  CAS PubMed Google Scholar
• Chapman, J. R. & Jackson, S. P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 9, 795–801 (2008).
  CAS PubMed PubMed Central Google Scholar
• Melander, F. et al. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 181, 213–226 (2008).
  CAS PubMed PubMed Central Google Scholar
• Spycher, C. et al. Constitutive phosphorylation of MDC1 physically links the MRE11–RAD50–NBS1 complex to damaged chromatin. J. Cell Biol. 181, 227–240 (2008).
  CAS PubMed PubMed Central Google Scholar
• Wu, L., Luo, K., Lou, Z. & Chen, J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl Acad. Sci. USA 105, 11200–11205 (2008).
  CAS PubMed PubMed Central Google Scholar
• Huen, M. S. et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901–914 (2007).
  CAS PubMed PubMed Central Google Scholar
• Kolas, N. K. et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637–1640 (2007).
  CAS PubMed PubMed Central Google Scholar
• Mailand, N. et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887–900 (2007).
  CAS PubMed Google Scholar
• Kim, H., Chen, J. & Yu, X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202–1205 (2007).
  CAS PubMed Google Scholar
• Sobhian, B. et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198–1202 (2007).
  CAS PubMed PubMed Central Google Scholar
• Wang, B. et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194–1198 (2007).
  CAS PubMed PubMed Central Google Scholar
• Lisby, M., Barlow, J. H., Burgess, R. C. & Rothstein, R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699–713 (2004). A comprehensive analysis of the temporal sequence of recruitment events in S. cerevisiae.
  CAS PubMed Google Scholar
• Melo, J. & Toczyski, D. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14, 237–245 (2002).
  CAS PubMed Google Scholar
• Bonilla, C. Y., Melo, J. A. & Toczyski, D. P. Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell 30, 267–276 (2008). Introduces the concept of activation of the DDR in the absence of DNA breaks in S. cerevisiae.
  CAS PubMed PubMed Central Google Scholar
• Soutoglou, E. DNA lesions and DNA damage response: Even long lasting relationships need a “break”. Cell Cycle 7, 3653–3658 (2008).
  CAS PubMed Google Scholar
• Soutoglou, E. & Misteli, T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320, 1507–1510 (2008). Introduces the concept of activation of the DDR in the absence of DNA breaks in mammalian cells.
  CAS PubMed PubMed Central Google Scholar
• Lukas, C., Bartek, J. & Lukas, J. Imaging of protein movement induced by chromosomal breakage: tiny 'local' lesions pose great 'global' challenges. Chromosoma 114, 146–154 (2005).
  CAS PubMed Google Scholar
• Bekker-Jensen, S. et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195–206 (2006).
  CAS PubMed PubMed Central Google Scholar
• Essers, J. et al. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21, 2030–2037 (2002).
  CAS PubMed PubMed Central Google Scholar
• Lukas, C. et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674–2683 (2004).
  CAS PubMed PubMed Central Google Scholar
• Gorski, S. A., Snyder, S. K., John, S., Grummt, I. & Misteli, T. Modulation of RNA polymerase assembly dynamics in transcriptional regulation. Mol. Cell 30, 486–497 (2008).
  CAS PubMed PubMed Central Google Scholar
• Politi, A. et al. Mathematical modeling of nucleotide excision repair reveals efficiency of sequential assembly strategies. Mol. Cell 19, 679–690 (2005). Reports the development of a mathematical model for the assembly process of the DNA-repair machinery in vivo.
  CAS PubMed Google Scholar
• Toledo, L. I., Murga, M., Gutierrez-Martinez, P., Soria, R. & Fernandez-Capetillo, O. ATR signaling can drive cells into senescence in the absence of DNA breaks. Genes Dev. 22, 297–302 (2008). Shows that a persistent DDR in the absence of breaks leads to cellular senescence.
  CAS PubMed PubMed Central Google Scholar
• Bakkenist, C. J. & Kastan, M. B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499–506 (2003).
  CAS PubMed Google Scholar
• Mazumdar, M. et al. Tumor formation via loss of a molecular motor protein. Curr. Biol. 16, 1559–1564 (2006).
  CAS PubMed PubMed Central Google Scholar
• Bencokova, Z. et al. ATM activation and signalling under hypoxic conditions. Mol. Cell. Biol. 29, 526–537 (2008).
  PubMed PubMed Central Google Scholar
• Downs, J. A., Nussenzweig, M. C. & Nussenzweig, A. Chromatin dynamics and the preservation of genetic information. Nature 447, 951–958 (2007).
  CAS PubMed Google Scholar
• Rogakou, E. P., Boon, C., Redon, C. & Bonner, W. M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146, 905–916 (1999).
  CAS PubMed PubMed Central Google Scholar
• Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858–5868 (1998).
  CAS PubMed Google Scholar
• Bassing, C. H. et al. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114, 359–370 (2003).
  CAS PubMed Google Scholar
• Celeste, A. et al. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114, 371–383 (2003). Demonstrates the functional importance of H2AX phosphorylation in genome maintenance.
  CAS PubMed PubMed Central Google Scholar
• Celeste, A. et al. Genomic instability in mice lacking histone H2AX. Science 296, 922–927 (2002).
  CAS PubMed PubMed Central Google Scholar
• Reina-San-Martin, B. et al. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med. 197, 1767–1778 (2003).
  CAS PubMed PubMed Central Google Scholar
• Xie, A. et al. Control of sister chromatid recombination by histone H2AX. Mol. Cell 16, 1017–1025 (2004).
  CAS PubMed Google Scholar
• Zhou, B. B. & Elledge, S. J. The DNA damage response: putting checkpoints in perspective. Nature 408, 433–439 (2000).
  CAS PubMed Google Scholar
• Celeste, A. et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biol. 5, 675–679 (2003).
  CAS PubMed Google Scholar
• Downs, J. A., Lowndes, N. F. & Jackson, S. P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408, 1001–1004 (2000).
  CAS PubMed Google Scholar
• Fernandez-Capetillo, O. et al. DNA damage-induced G2–M checkpoint activation by histone H2AX and 53BP1. Nature Cell Biol. 4, 993–997 (2002).
  CAS PubMed Google Scholar
• Downs, J. A. et al. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16, 979–990 (2004).
  CAS PubMed Google Scholar
• Kusch, T. et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306, 2084–2087 (2004).
  CAS PubMed Google Scholar
• Morrison, A. J. et al. INO80 and γ-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767–775 (2004).
  CAS PubMed Google Scholar
• Unal, E. et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16, 991–1002 (2004).
  PubMed Google Scholar
• van Attikum, H., Fritsch, O., Hohn, B. & Gasser, S. M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119, 777–788 (2004).
  CAS PubMed Google Scholar
• Kruhlak, M. J. et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172, 823–834 (2006).
  CAS PubMed PubMed Central Google Scholar
• Ziv, Y. et al. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nature Cell Biol. 8, 870–876 (2006).
  CAS PubMed Google Scholar
• Bao, Y. & Shen, X. Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17, 126–131 (2007).
  CAS PubMed Google Scholar
• Chai, B., Huang, J., Cairns, B. R. & Laurent, B. C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656–1661 (2005).
  CAS PubMed PubMed Central Google Scholar
• Tsukuda, T., Fleming, A. B., Nickoloff, J. A. & Osley, M. A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438, 379–383 (2005).
  CAS PubMed PubMed Central Google Scholar
• Kobor, M. S. et al. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2, E131 (2004).
  PubMed PubMed Central Google Scholar
• Mizuguchi, G. et al. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343–348 (2004).
  CAS PubMed Google Scholar
• Papamichos-Chronakis, M., Krebs, J. E. & Peterson, C. L. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20, 2437–2449 (2006).
  CAS PubMed PubMed Central Google Scholar
• van Attikum, H., Fritsch, O. & Gasser, S. M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26, 4113–4125 (2007).
  CAS PubMed PubMed Central Google Scholar
• Park, J. H. et al. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting γ-H2AX induction. EMBO J. 25, 3986–3997 (2006).
  CAS PubMed PubMed Central Google Scholar
• Haldar, D. & Kamakaka, R. T. Schizosaccharomyces pombe Hst4 functions in DNA damage response by regulating histone H3 K56 acetylation. Eukaryot. Cell 7, 800–813 (2008).
  CAS PubMed PubMed Central Google Scholar
• Jazayeri, A., McAinsh, A. D. & Jackson, S. P. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl Acad. Sci. USA 101, 1644–1649 (2004).
  CAS PubMed PubMed Central Google Scholar
• Tamburini, B. A. & Tyler, J. K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25, 4903–4913 (2005).
  CAS PubMed PubMed Central Google Scholar
• Keogh, M. C. et al. A phosphatase complex that dephosphorylates γH2AX regulates DNA damage checkpoint recovery. Nature 439, 497–501 (2006).
  CAS PubMed Google Scholar
• Chowdhury, D. et al. γ-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20, 801–809 (2005).
  CAS PubMed Google Scholar
• Chowdhury, D. et al. A PP4-phosphatase complex dephosphorylates γ-H2AX generated during DNA replication. Mol. Cell 31, 33–46 (2008).
  CAS PubMed PubMed Central Google Scholar
• Krogan, N. J. et al. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc. Natl Acad. Sci. USA 101, 13513–13518 (2004).
  CAS PubMed PubMed Central Google Scholar
• Ikura, T. et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27, 7028–7040 (2007).
  CAS PubMed PubMed Central Google Scholar
• Jha, S., Shibata, E. & Dutta, A. Human Rvb1/Tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol. Cell. Biol. 28, 2690–2700 (2008).
  CAS PubMed PubMed Central Google Scholar
• Heo, K. et al. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 30, 86–97 (2008).
  CAS PubMed Google Scholar
• Polo, S. E., Roche, D. & Almouzni, G. New histone incorporation marks sites of UV repair in human cells. Cell 127, 481–493 (2006).
  CAS PubMed Google Scholar
• Chen, C. C. et al. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134, 231–243 (2008).
  CAS PubMed PubMed Central Google Scholar
• Mousson, F., Ochsenbein, F. & Mann, C. The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116, 79–93 (2007).
  CAS PubMed Google Scholar
• Tyler, J. K. et al. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402, 555–560 (1999).
  CAS PubMed Google Scholar
• Mello, J. A. et al. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3, 329–334 (2002).
  CAS PubMed PubMed Central Google Scholar
• O'Hagan, H. M., Mohammad, H. P. & Baylin, S. B. Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet. 4, e1000155 (2008).
  PubMed PubMed Central Google Scholar
• Oberdoerffer, P. et al. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 135, 907–918 (2008).
  CAS PubMed PubMed Central Google Scholar
• Goodarzi, A. A. et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31, 167–177 (2008). Provides evidence for a role of higher-order chromatin structure in DDR activation.
  CAS PubMed Google Scholar
• Ayoub, N., Jeyasekharan, A. D., Bernal, J. A. & Venkitaraman, A. R. HP1-β mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453, 682–686 (2008).
  CAS PubMed Google Scholar
• Kim, Y. C. et al. The activation of ATM depends on chromatin interactions occurring prior to DNA damage induction. Nature Cell Biol. 11, 92–96 (2008).
  PubMed Google Scholar
• Murga, M. et al. Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol. 178, 1101–1108 (2007). Provides evidence for an inhibitory effect of chromatin compaction on DNA-damage signalling.
  CAS PubMed PubMed Central Google Scholar
• Kim, J. A., Kruhlak, M., Dotiwala, F., Nussenzweig, A. & Haber, J. E. Heterochromatin is refractory to γ-H2AX modification in yeast and mammals. J. Cell Biol. 178, 209–218 (2007).
  CAS PubMed PubMed Central Google Scholar
• Efroni, S. et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437–447 (2008).
  CAS PubMed PubMed Central Google Scholar
• Lisby, M., Antunez de Mayolo, A., Mortensen, U. H. & Rothstein, R. Cell cycle-regulated centers of DNA double-strand break repair. Cell Cycle 2, 479–483 (2003).
  CAS PubMed Google Scholar
• Lisby, M., Mortensen, U. H. & Rothstein, R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nature Cell Biol. 5, 572–577 (2003).
  CAS PubMed Google Scholar
• Lisby, M. & Rothstein, R. DNA damage checkpoint and repair centers. Curr. Opin. Cell Biol. 16, 328–334 (2004).
  CAS PubMed Google Scholar
• Nagai, S. et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322, 597–602 (2008).
  CAS PubMed PubMed Central Google Scholar
• Soutoglou, E. et al. Positional stability of single double-strand breaks in mammalian cells. Nature Cell Biol. 9, 675–682 (2007). Reports the development and use of an experimental system to visualize DSBs in living mammalian cells and demonstrates that mammalian DSBs are immobile in the cell nucleus.
  CAS PubMed Google Scholar
• Aten, J. A. et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303, 92–95 (2004).
  CAS PubMed Google Scholar
• Nelms, B. E., Maser, R. S., MacKay, J. F., Lagally, M. G. & Petrini, J. H. In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280, 590–592 (1998).
  CAS PubMed Google Scholar
• Dimitrova, N., Chen, Y. C., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524–528 (2008). Shows that 53BP1 promotes chromatin mobility and end joining of deprotected telomeres.
  CAS PubMed PubMed Central Google Scholar
• Difilippantonio, S. et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 456, 529–533 (2008).
  CAS PubMed PubMed Central Google Scholar
• Soutoglou, E. & Misteli, T. Mobility and immobility of chromatin in transcription and genome stability. Curr. Opin. Genet. Dev. 17, 435–442 (2007).
  CAS PubMed PubMed Central Google Scholar
• Lanctot, C., Cheutin, T., Cremer, M., Cavalli, G. & Cremer, T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nature Rev. Genet. 8, 104–115 (2007).
  CAS PubMed Google Scholar
• Meaburn, K. J. & Misteli, T. Cell biology: chromosome territories. Nature 445, 379–781 (2007).
  CAS PubMed Google Scholar
• Meaburn, K. J., Misteli, T. & Soutoglou, E. Spatial genome organization in the formation of chromosomal translocations. Semin. Cancer Biol. 17, 80–90 (2007).
  CAS PubMed Google Scholar
• Liyanage, M. et al. Abnormal rearrangement within the α/δ T-cell receptor locus in lymphomas from Atm-deficient mice. Blood 96, 1940–1946 (2000).
  CAS PubMed Google Scholar
• Parada, L. A., McQueen, P. G., Munson, P. J. & Misteli, T. Conservation of relative chromosome positioning in normal and cancer cells. Curr. Biol. 12, 1692–1697 (2002).
  CAS PubMed Google Scholar
• Parada, L. A., McQueen, P. G. & Misteli, T. Tissue-specific spatial organization of genomes. Genome Biol. 5, R44 (2004).
  PubMed PubMed Central Google Scholar
• Neves, H., Ramos, C., da Silva, M. G., Parreira, A. & Parreira, L. The nuclear topography of ABL, BCR, PML, and RARα genes: evidence for gene proximity in specific phases of the cell cycle and stages of hematopoietic differentiation. Blood 93, 1197–1207 (1999).
  CAS PubMed Google Scholar
• Roix, J. J., McQueen, P. G., Munson, P. J., Parada, L. A. & Misteli, T. Spatial proximity of translocation-prone gene loci in human lymphomas. Nature Genet. 34, 287–291 (2003). Demonstrates a correlation between the spatial proximity of genome regions and their likelihood of translocating, pointing to a significant role of non-random genome organization in determining translocation outcome.
  CAS PubMed Google Scholar
• Branco, M. R. & Pombo, A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 4, e138 (2006). Demonstrates physical intermingling of the chromatin fibres of neighbouring chromosomes.
  PubMed PubMed Central Google Scholar
• Mitelman, F., Johansson, B. & Mertens, F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nature Genet. 36, 331–334 (2004).
  CAS PubMed Google Scholar
• Bird, A. W. et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419, 411–415 (2002).
  CAS PubMed Google Scholar
• Megee, P. C., Morgan, B. A. & Smith, M. M. Histone H4 and the maintenance of genome integrity. Genes Dev. 9, 1716–1727 (1995).
  CAS PubMed Google Scholar
• Qin, S. & Parthun, M. R. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell. Biol. 22, 8353–8365 (2002).
  CAS PubMed PubMed Central Google Scholar
• Qin, S. & Parthun, M. R. Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol. Cell. Biol. 26, 3649–3658 (2006).
  CAS PubMed PubMed Central Google Scholar
• Murr, R. et al. Histone acetylation by Trrap–Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nature Cell Biol. 8, 91–99 (2006).
  CAS PubMed Google Scholar
• Murr, R., Vaissiere, T., Sawan, C., Shukla, V. & Herceg, Z. Orchestration of chromatin-based processes: mind the TRRAP. Oncogene 26, 5358–5372 (2007).
  CAS PubMed Google Scholar
• Gupta, A. et al. Involvement of human MOF in ATM function. Mol. Cell. Biol. 25, 5292–5305 (2005).
  CAS PubMed PubMed Central Google Scholar
• Driscoll, R., Hudson, A. & Jackson, S. P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315, 649–652 (2007).
  CAS PubMed PubMed Central Google Scholar
• Masumoto, H., Hawke, D., Kobayashi, R. & Verreault, A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436, 294–298 (2005).
  CAS PubMed Google Scholar
• Huyen, Y. et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406–411 (2004).
  CAS PubMed Google Scholar
• Wysocki, R. et al. Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25, 8430–8443 (2005).
  CAS PubMed PubMed Central Google Scholar
• Botuyan, M. V. et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361–1373 (2006).
  CAS PubMed PubMed Central Google Scholar
• Houston, S. I. et al. Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J. Biol. Chem. 283, 19478–19488 (2008).
  CAS PubMed PubMed Central Google Scholar
• Jorgensen, S. et al. The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179, 1337–1345 (2007).
  PubMed PubMed Central Google Scholar
• Du, L. L., Nakamura, T. M. & Russell, P. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20, 1583–1596 (2006).
  CAS PubMed PubMed Central Google Scholar
• Sanders, S. L. et al. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603–614 (2004).
  CAS PubMed Google Scholar
• Fernandez-Capetillo, O., Allis, C. D. & Nussenzweig, A. Phosphorylation of histone H2B at DNA double-strand breaks. J. Exp. Med. 199, 1671–1677 (2004).
  CAS PubMed PubMed Central Google Scholar
• Ahn, S. H., Henderson, K. A., Keeney, S. & Allis, C. D. H2B (Ser10) phosphorylation is induced during apoptosis and meiosis in S. cerevisiae. Cell Cycle 4, 780–783 (2005).
  CAS PubMed Google Scholar