Skip to main content
SpringerLink
Log in

Chromatin: The Entry to and Exit from DNA Repair

  • Chapter
  • First Online:
Post-Translational Modifications in Health and Disease

Part of the book series: Protein Reviews ((PRON,volume 13))

  • 1320 Accesses

Abstract

All processes of DNA metabolism require a high degree of coordination with the processes that modify chromatin structure. Recent experimental efforts have established that post-translational modifications of histones and chromatin remodeling activities are required for DNA repair. Dynamic changes of chromatin are the means to control accessibility, coordinate binding of repair and signaling proteins and link DNA repair with the cell cycle. In this review, we focus on current understanding of the roles of histone modifications and chromatin remodeling events in repair of different DNA lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahnesorg, P., Smith, P., Jackson, S.P., et al. (2006). XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124:301–313.

    PubMed  CAS  Google Scholar 

  • Allison, S.J., and Milner, J. (2004). Remodelling chromatin on a global scale: a novel protective function of p53. Carcinogenesis 25:1551–1557.

    PubMed  CAS  Google Scholar 

  • Bao, Y., and Shen, X. (2007a). Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17:126–131.

    PubMed  CAS  Google Scholar 

  • Bao, Y., and Shen, X. (2007b). INO80 subfamily of chromatin remodeling complexes. Mutat. Res. 618:18–29.

    PubMed  CAS  Google Scholar 

  • Batty, D.P., and Wood, R.D. (2000). Damage recognition in nucleotide excision repair of DNA. Gene 241:193–204.

    PubMed  CAS  Google Scholar 

  • Beard, B.C., Wilson, S.H., Smerdon, M.J. (2003). Suppressed catalytic activity of base excision repair enzymes on rotationally positioned uracil in nucleosomes. Proc. Natl. Acad. Sci. USA. 100:7465–7470.

    PubMed  CAS  Google Scholar 

  • Bekker-Jensen, S., Lukas, C., Melander, F., et al. (2005). Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170:201–211.

    PubMed  CAS  Google Scholar 

  • Bekker-Jensen, S., Lukas, C., Kitagawa, R., et al. (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173: 195–206.

    PubMed  CAS  Google Scholar 

  • Bird, A.W., Yu, D.Y., Pray-Grant, M.G., et al. (2002). Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419:411–415.

    PubMed  CAS  Google Scholar 

  • Bochar, D.A., Wang, L., Beniya, H., et al. (2000). BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 102:257–265.

    PubMed  CAS  Google Scholar 

  • Bohr, V.A., Smith, C.A., Okumoto, D.S., et al. (1985). DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359–369.

    PubMed  CAS  Google Scholar 

  • Bonner, W.M., Redon, C.E., Dickey, J.S., et al. (2008). GammaH2AX and cancer. Nat. Rev. Cancer 8:957–967.

    PubMed  CAS  Google Scholar 

  • Bostelman, L.J., Keller, A.M., Albrecht A.M., et al. (2007). Methylation of histone H3 lysine-79 by Dot1p plays multiple roles in the response to UV damage in Saccharomyces cerevisiae. DNA Repair (Amst) 6:383–395.

    CAS  Google Scholar 

  • Brand, M., Moggs, J.G., Oulad-Abdelghani, M., et al. (2001). UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J. 20:3187–3196.

    PubMed  CAS  Google Scholar 

  • Bucceri, A., Kapitza, K., Thoma, F. (2006). Rapid accessibility of nucleosomal DNA in yeast on a second time scale. EMBO J. 25:3123–3132.

    PubMed  CAS  Google Scholar 

  • Bugreev, D.V, Mazina, O.M, Mazin, A.V., et al. (2006). Rad54 protein promotes branch migration of Holliday junctions. Nature 442:590–593.

    PubMed  CAS  Google Scholar 

  • Burma, S., and Chen, D.J. (2004). Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst) 3:909–918.

    CAS  Google Scholar 

  • Burma, S., Chen, B.P., Murphy, M., et al. (2001). ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:42462–42467.

    PubMed  CAS  Google Scholar 

  • Cannavo, E., Gerrits, B., Marra, G., et al. (2007). Characterization of the interactome of the human MutL homologues MLH1, PMS1, and PMS2. J. Biol. Chem. 282:2976–2986.

    PubMed  CAS  Google Scholar 

  • Celeste, A., Fernandez-Capetillo, O., Kruhlak, M.J., et al. (2003). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675–679.

    PubMed  CAS  Google Scholar 

  • Chai, B., Huang, J., Cairns, B.R., et al. (2005). Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes. Dev. 19:1656–1661.

    PubMed  CAS  Google Scholar 

  • Cheung, K. J. Jr., Mitchell, D., Lin, P., et al. (2001). The tumor suppressor candidate p33(ING1) mediates repair of UV-damaged DNA. Cancer Res. 61:4974–4977.

    PubMed  CAS  Google Scholar 

  • Cheung, W.L, Turner, F.B., Krishnamoorthy T., et al. (2005). Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr. Biol. 15:656–660.

    PubMed  CAS  Google Scholar 

  • Chowdhury, D., Keogh, M.C., Ishii, H., et al. (2005). Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20:801–809.

    PubMed  CAS  Google Scholar 

  • Cortez, D., Guntuku, S., Qin, J., et al. (2001). ATR and ATRIP: partners in checkpoint signaling. Science 294:1713–1716.

    PubMed  CAS  Google Scholar 

  • Datta, A., Bagchi, S., Nag, A., et al. (2001). The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat. Res. 486:89–97.

    PubMed  CAS  Google Scholar 

  • Downs. J.A., Lowndes, N.F., Jackson, S.P., et al. (2000). A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001–1004.

    PubMed  CAS  Google Scholar 

  • Downs, J. A., Allard, S., Jobin-Robitaille, O., et al. (2004). Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16:979–990.

    PubMed  CAS  Google Scholar 

  • Doyon. Y., Cayrou, C., Ullah, M., et al. (2006). ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 21:51–64.

    PubMed  CAS  Google Scholar 

  • Escargueil, A.E., Soares, D.G, Salvador, M., et al. (2008). What histone code for DNA repair? Mutat. Res. 658:259–270.

    CAS  Google Scholar 

  • Evans, D.H., and Linn, S. (1984). Excision repair of pyrimidine dimers from simian virus 40 minichromosomes in vitro. J. Biol. Chem. 259:10252–10259.

    PubMed  CAS  Google Scholar 

  • Evans, M.L., Bostelman, L. J., Albrecht, A.M., et al. (2008). UV sensitive mutations in histone H3 in Saccharomyces cerevisiae that alter specific K79 methylation states genetically act through distinct DNA repair pathways. Curr. Genet. 53:259–274.

    PubMed  CAS  Google Scholar 

  • Falck, J., Coates, J., Jackson, S.P. (2005). Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–611.

    PubMed  CAS  Google Scholar 

  • Falk, M., Lukasova, E., Gabrielova, B., et al. (2007). Chromatin dynamics during DSB repair. Biochim. Biophys. Acta 1773:1534–1545.

    PubMed  CAS  Google Scholar 

  • Fernandez-Capetillo, O., Allis, C.D., Nussenzweig, A. (2004). Phosphorylation of histone H2B at DNA double-strand breaks. J. Exp. Med. 199:1671–1677.

    PubMed  CAS  Google Scholar 

  • Flores-Rozas, H., Clark, D., Kolodner, R.D. (2000). Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex. Nat. Genet. 26:375–378.

    PubMed  CAS  Google Scholar 

  • Fortini, P., and Dogliotti, E. (2007). Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst) 6:398–409.

    CAS  Google Scholar 

  • Fritsch, O., Benvenuto, G. Bowler, C., et al. (2004). The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16:479–485.

    PubMed  CAS  Google Scholar 

  • Goodarzi, A.A., Noon, A.T., Deckbar, D., et al. (2008). ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31:167–177.

    PubMed  CAS  Google Scholar 

  • Gospodinov, A., Tsaneva, I., Anachkova, B. (2009). RAD51 foci formation in response to DNA damage is modulated by TIP49. Int. J. Biochem. Cell. Biol. 41:925–933.

    PubMed  CAS  Google Scholar 

  • Gravel, S., Chapman, J.R. Magill, C., et al. (2008). DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22:2767–2772.

    PubMed  CAS  Google Scholar 

  • Groth, A., Rocha, W., Verreault, A., et al. (2007). Chromatin challenges during DNA replication and repair. Cell 128:721–733.

    PubMed  CAS  Google Scholar 

  • Hanawalt, P. C. (2002). Subpathways of nucleotide excision repair and their regulation. Oncogene 21:8949–8956.

    PubMed  CAS  Google Scholar 

  • Hara, R. and Sancar, A. (2002). The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol. Cell. Biol. 22:6779–6787.

    PubMed  CAS  Google Scholar 

  • Hara, R., and Sancar, A. (2003). Effect of damage type on stimulation of human excision nuclease by SWI/SNF chromatin remodeling factor. Mol. Cell. Biol. 23:4121–4125.

    PubMed  CAS  Google Scholar 

  • Hasan, S., Hassa, P.O., Imhof, R., et al. (2001). Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 410:387–391.

    PubMed  CAS  Google Scholar 

  • Helleday, T., Petermann, E., Lundin, C., et al. (2008). DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8:193–204.

    PubMed  CAS  Google Scholar 

  • Herceg, Z. (2007). Epigenetics and cancer: towards an evaluation of the impact of environmental and dietary factors. Mutagenesis 22:91–103.

    PubMed  CAS  Google Scholar 

  • Huang, J., Liang, B., Qiu, J., et al. (2005). ATP-dependent chromatin-remodeling complexes in DNA double-strand break repair: remodeling, pairing and (re)pairing. Cell Cycle 4:1713–1715.

    PubMed  CAS  Google Scholar 

  • Huggins, C.F., Chafin, D.R., Aoyagi, S., et al. (2002). Flap endonuclease 1 efficiently cleaves base excision repair and DNA replication intermediates assembled into nucleosomes. Mol. Cell 10:1201–1211.

    PubMed  CAS  Google Scholar 

  • Huyen, Y., Zgheib, O., DiTullio, R.A., et al. (2004). Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406–411.

    PubMed  CAS  Google Scholar 

  • Ikura, T., Ogryzko, V.V., Grigoriev, M., et al. (2000). Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463–473.

    PubMed  CAS  Google Scholar 

  • Ikura, T., Tashiro, S., Kakino, A., et al. (2007). DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27:7028–7040.

    PubMed  CAS  Google Scholar 

  • Ip, S.C., Rass, U., Blanco, M.G., et al. (2008). Identification of Holliday junction resolvases from humans and yeast. Nature 456:357–361.

    PubMed  CAS  Google Scholar 

  • Ira, G., Pellicioli, A., Balijja, A., et al. (2004). DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011–1017.

    PubMed  CAS  Google Scholar 

  • Jha, S., Shibata, E., Dutta, A., et al. (2008). 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.

    PubMed  CAS  Google Scholar 

  • Keogh, M.C., Kim, J.A., Downey, M., et al. (2006). A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439:497–501.

    PubMed  CAS  Google Scholar 

  • Kim, Y.C., Gerlitz, G., Furusawa, T., et al. (2009). Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat. Cell Biol. 11:92–96.

    PubMed  CAS  Google Scholar 

  • Kinner, A., Wu, W., Iliakis, G. (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36:5678–5694.

    PubMed  CAS  Google Scholar 

  • Kleczkowska, H.E., Marra, G., Lettieri, T., et al. (2001). hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci. Genes Dev. 15:724–736.

    PubMed  CAS  Google Scholar 

  • Klochendler-Yeivin, A., Picarsky, E., Yaniv, M. (2006). Increased DNA damage sensitivity and apoptosis in cells lacking the Snf5/Ini1 subunit of the SWI/SNF chromatin remodeling complex. Mol. Cell. Biol. 26:2661–2674.

    PubMed  CAS  Google Scholar 

  • Kobayashi, J., Tauchi, H., Sakamoto, S., et al. (2002). NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12:1846–1851.

    PubMed  CAS  Google Scholar 

  • Kobor, M.S., Venkatasubrahmanyam, S., Moneghini, M.D., et al. (2004). A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2:E131.

    PubMed  Google Scholar 

  • Krogan, N.J., Keogh, M.C., Datta, N., et al. (2003). A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12:1565–1576.

    PubMed  CAS  Google Scholar 

  • Kruhlak, M.J., Celeste, A., Dellaire, G., et al. (2006). Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172:823–834.

    PubMed  CAS  Google Scholar 

  • Kuo, W.H., Wang, Y., Wong, R.P., et al. (2007). The ING1b tumor suppressor facilitates nucleotide excision repair by promoting chromatin accessibility to XPA. Exp. Cell Res. 313:1628–1638.

    PubMed  CAS  Google Scholar 

  • Kusch, T., Florens, L., Macdonald, W.H., et al. (2004). Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084–2087.

    PubMed  CAS  Google Scholar 

  • Kwon, J., Morshead, K.B., Guyon, J.R., et al. (2000). Histone acetylation and hSWI/SNF remodeling act in concert to stimulate V(D)J cleavage of nucleosomal DNA. Mol. Cell 6:1037–1048.

    PubMed  CAS  Google Scholar 

  • Lan, S.Y., and Smerdon, M.J. (1985). A nonuniform distribution of excision repair synthesis in nucleosome core DNA. Biochemistry 24:7771–7783.

    PubMed  CAS  Google Scholar 

  • Lazzaro, F., Sapountzi, V., Granata, M., et al. (2008). Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 27:1502–1512.

    PubMed  CAS  Google Scholar 

  • Lee, J.H., and Paull, T.T. (2005). ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551–554.

    PubMed  CAS  Google Scholar 

  • Lees-Miller, S.P., and Meek, K. (2003). Repair of DNA double strand breaks by non-homologous end joining. Biochimie 85:1161–1173.

    PubMed  CAS  Google Scholar 

  • Li, B., Pattenden, S.G., Lee, D., et al. (2005). Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc. Natl. Acad. Sci. USA. 102:18385–18390.

    PubMed  CAS  Google Scholar 

  • Liang, B., Qiu, J., Ratnakumar, K., et al. (2007). RSC functions as an early double-strand-break sensor in the cell’s response to DNA damage. Curr. Biol. 17:1432–1437.

    PubMed  CAS  Google Scholar 

  • Limbo, O., Chahwan, C., Yamada, Y., et al. (2007). Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28:134–146.

    PubMed  CAS  Google Scholar 

  • Ljungman, M., and Lane, D.P. (2004). Transcription - guarding the genome by sensing DNA damage. Nat. Rev. Cancer 4:727–737.

    PubMed  CAS  Google Scholar 

  • Lukas, C., Melander, F., Stucki, M., et al. (2004). Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23:2674–2683.

    PubMed  CAS  Google Scholar 

  • Martinez, E., Palhan, V.B., Tjernberg, A., et al. (2001). Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 21:6782–6795.

    PubMed  CAS  Google Scholar 

  • Mellon, I., Spivak, G., Hanawalt, P.C. (1987). Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51:241–249.

    PubMed  CAS  Google Scholar 

  • Meneghini, M.D, Wu, M., Medhani, H.D. (2003). Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112:725–736.

    PubMed  CAS  Google Scholar 

  • Menoni, H., Gasparutto, D., Hamiche, A., et al. (2007). ATP-dependent chromatin remodeling is required for base excision repair in conventional but not in variant H2A.Bbd nucleosomes. Mol. Cell. Biol. 27:5949–5956.

    PubMed  CAS  Google Scholar 

  • Mimitou, E.P., and Symington, L.S. (2008). Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–774.

    PubMed  CAS  Google Scholar 

  • Mizuguchi, G., Shen, X., Landry, J., et al. (2004). ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343–348.

    PubMed  CAS  Google Scholar 

  • Modesti, M., Junop, M.S., Ghirlando, R., et al. (2003). Tetramerization and DNA ligase IV interaction of the DNA double-strand break repair protein XRCC4 are mutually exclusive. J. Mol. Biol. 334:215–228.

    PubMed  CAS  Google Scholar 

  • Morrison, A.J., Highland, J., Krogan, N.J., et al. (2004). INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767–775.

    PubMed  CAS  Google Scholar 

  • Morshead, K.B., Ciccone, D.N., Taverna, S.D., et al. (2003). Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl. Acad. Sci. USA. 100:11577–11582.

    PubMed  CAS  Google Scholar 

  • Moynahan, M.E., Chiu, J.W., Koller, B.H., et al. (1999). Brca1 controls homology-directed DNA repair. Mol. Cell 4:511–518.

    PubMed  CAS  Google Scholar 

  • Murr, R., Loizou, J.I., Yang, Y.G., et al. (2006). Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell. Biol. 8:91–99.

    PubMed  CAS  Google Scholar 

  • Nakada, D., Hirano, Y., Sugimoto, K., et al. (2004). Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway. Mol. Cell. Biol. 24:10016–10025.

    PubMed  CAS  Google Scholar 

  • New, J.H., Sugiyama, T., Zaitseva, E., et al. (1998). Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391:407–410.

    PubMed  CAS  Google Scholar 

  • Papamichos-Chronakis, M., Krebs, J.E., Peterson, C.L., et al. (2006). Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20:2437–2449.

    PubMed  CAS  Google Scholar 

  • Paques, F., and Haber, J.E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349–404.

    PubMed  CAS  Google Scholar 

  • Patenge, N., Elkin, S.K., Oettinger, M.A. (2004). ATP-dependent remodeling by SWI/SNF and ISWI proteins stimulates V(D)J cleavage of 5 S arrays. J. Biol. Chem. 279:35360–35367.

    PubMed  CAS  Google Scholar 

  • Paull T.T., Rogakou, E.P, Yamazaki, V., et al. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:886–895.

    PubMed  CAS  Google Scholar 

  • Petukhova, G., Stratton, S., Sung, P. (1998). Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393:91–94.

    PubMed  CAS  Google Scholar 

  • Ramanathan, B., and Smerdon, M.J. (1986). Changes in nuclear protein acetylation in u.v.-damaged human cells. Carcinogenesis 7:1087–1094.

    PubMed  CAS  Google Scholar 

  • Ramanathan, B. and Smerdon, M.J. (1989). Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J. Biol. Chem. 264:11026–11034.

    PubMed  CAS  Google Scholar 

  • Rappold, I., Iwabuchi. K., Date, T., et al. (2001). Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153:613–620.

    PubMed  CAS  Google Scholar 

  • Resnick. M.A., and Martin, P. (1976). The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol. Gen. Genet. 143:119–129.

    PubMed  CAS  Google Scholar 

  • Richardson, C., Moynahan, M.E., Jasin, M. (1998). Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831–3842.

    PubMed  CAS  Google Scholar 

  • Robert, F., Hardy, S., Nagy, Z., et al. (2006). The transcriptional histone acetyltransferase cofactor TRRAP associates with the MRN repair complex and plays a role in DNA double-strand break repair. Mol. Cell. Biol. 26:402–412.

    PubMed  CAS  Google Scholar 

  • Rogakou, E.P., Boon, C., Redon, C., et al. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905–916.

    PubMed  CAS  Google Scholar 

  • Rubbi, C.P., and Milner, J. (2003). p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J. 22:975–986.

    PubMed  CAS  Google Scholar 

  • Sancar, A., Lindsey-Boltz, L.A., Unsal-Kaçmaz, K. et al. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39–85.

    PubMed  CAS  Google Scholar 

  • Sanders, S.L., Portoso, M., Mata, J., et al. (2004). Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603–614.

    PubMed  CAS  Google Scholar 

  • Schotta, G., Sengupta, R., Kubicek, S., et al. (2008). A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22:2048–2061.

    PubMed  CAS  Google Scholar 

  • Shen, Z., Cloud, K.G, Chen, D.J., et al. (1996). Specific interactions between the human RAD51 and RAD52 proteins. J. Biol. Chem. 271:148–152.

    PubMed  CAS  Google Scholar 

  • Shen, X., Mizuguchi, G., Hamiche, A., et al. (2000). A chromatin remodelling complex involved in transcription and DNA processing. Nature 406:541–544.

    PubMed  CAS  Google Scholar 

  • Shen, X., Ranallo, R., Choi, E., et al. (2003). Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12:147–155.

    PubMed  CAS  Google Scholar 

  • Shiloh, Y. (2003). ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155–168.

    PubMed  CAS  Google Scholar 

  • Shim, E.Y., Ma, J.L., Oum J.H., et al. (2005). The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25:3934–3944.

    PubMed  CAS  Google Scholar 

  • Shim, E.Y., Hong, S.J., Oum J.H., et al. (2007). RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27:1602–1613.

    PubMed  CAS  Google Scholar 

  • Shinohara, A., Shinohara, M., Ohta, T., et al. (1998). Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3:145–156.

    PubMed  CAS  Google Scholar 

  • Shroff, R., Arbel-Eden, A., Sattler, U., et al. (2004). Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703–1711.

    PubMed  CAS  Google Scholar 

  • Sigurdsson, S., Van Komen, S., Petukhova, G., et al. (2002). Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem. 277:42790–42794.

    PubMed  CAS  Google Scholar 

  • Smerdon, M.J., and Lieberman, M.W. (1978). Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. Proc. Natl. Acad. Sci. USA. 75:4238–4241.

    PubMed  CAS  Google Scholar 

  • Soutoglou, E., and Misteli, T. (2008a). Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320:1507–1510.

    PubMed  CAS  Google Scholar 

  • Soutoglou, E., and Misteli, T. (2008b). On the contribution of spatial genome organization to cancerous chromosome translocations. J. Natl. Cancer Inst. Monogr. (39):16–19.

    PubMed  CAS  Google Scholar 

  • Soutoglou, E., Dorn, J.F., Sengupta, K., et al. (2007). Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9:675–682.

    PubMed  CAS  Google Scholar 

  • Stewart, G.S., Wang, B., Bignell, C.R., et al. (2003). MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961–966.

    PubMed  CAS  Google Scholar 

  • Stiff, T., O’Driscoll, M., Rief, N., et al. (2004). ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64:2390–2396.

    PubMed  CAS  Google Scholar 

  • Stucki, M., and Jackson, S.P. (2006). gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst) 5:534–543.

    CAS  Google Scholar 

  • Stucki, M., Clapperton, J.A., Mohammad, D., et al. (2005). MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213–1226.

    PubMed  CAS  Google Scholar 

  • Svejstrup, J.Q. (2002). Mechanisms of transcription-coupled DNA repair. Nat. Rev. Mol. Cell. Biol. 3:21–29.

    PubMed  CAS  Google Scholar 

  • Tamburini, B.A., and Tyler, J.K. (2005). Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25:4903–4913.

    PubMed  CAS  Google Scholar 

  • Tardat, M., Murr, R., Herceq, Z., et al. (2007). PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol. 179:1413–1426.

    PubMed  CAS  Google Scholar 

  • Teng, Y., Yu, Y., Waters, R., et al. (2002). The Saccharomyces cerevisiae histone acetyltransferase Gcn5 has a role in the photoreactivation and nucleotide excision repair of UV-induced cyclobutane pyrimidine dimers in the MFA2 gene. J. Mol. Biol. 316:489–499.

    PubMed  CAS  Google Scholar 

  • Thompson, L.H., and Schild, D. (2001). Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat. Res. 477:131–153.

    PubMed  CAS  Google Scholar 

  • Tini, M., Benecke, A., Um, S.J., et al. (2002). Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell 9:265–277.

    PubMed  CAS  Google Scholar 

  • Toh, G.W., O’Shaughnessy, A.M., Jimeno, S.J., et al. (2006). Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair (Amst) 5:693–703.

    CAS  Google Scholar 

  • Tsukuda, T., Fleming, A.B., Nickoloff, J.A., et al. (2005). Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379–383.

    PubMed  CAS  Google Scholar 

  • Ura, K., Araki, M., Saeki, H., et al. (2001). ATP-dependent chromatin remodeling facilitates nucleotide excision repair of UV-induced DNA lesions in synthetic dinucleosomes. EMBO J. 20:2004–2014.

    PubMed  CAS  Google Scholar 

  • Utley, R.T., Lacoste, N., Jobin-Robitaille, O., et al. (2005). Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell. Biol. 25:8179–8190.

    PubMed  CAS  Google Scholar 

  • van Attikum, H., Fritsch, O., Hohn, B., et al. (2004). Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777–788.

    PubMed  Google Scholar 

  • van Attikum, H., Fritsch, O., Gasser, S.M. (2007). Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26:4113–41125.

    PubMed  Google Scholar 

  • Volker, M., Mone, M.J., Karmakar, P., et al. (2001). Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8: 213–224.

    PubMed  CAS  Google Scholar 

  • Wakasugi, M., Kawashima, A., Morioka, H., et al. (2002). DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277:1637–1640.

    PubMed  CAS  Google Scholar 

  • Wang, J., Chin, M.Y., Li, G. (2006a). The novel tumor suppressor p33ING2 enhances nucleotide excision repair via inducement of histone H4 acetylation and chromatin relaxation. Cancer Res. 66:1906–1911.

    PubMed  CAS  Google Scholar 

  • Wang, Y., Wang, J., Li, G. (2006b). Leucine zipper-like domain is required for tumor suppressor ING2-mediated nucleotide excision repair and apoptosis. FEBS Lett. 580: 3787–3793.

    PubMed  CAS  Google Scholar 

  • Ward, I.M., and Chen, J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276: 47759–47762.

    PubMed  CAS  Google Scholar 

  • West, S.C. (2003). Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell. Biol. 4:435–445.

    PubMed  CAS  Google Scholar 

  • Wilkins, R.J. and Hart, R.W. (1974). Preferential DNA repair in human cells. Nature 247: 35–36.

    PubMed  CAS  Google Scholar 

  • Wong, L.Y, Recht, J., Laurent, B.C. (2006). Chromatin remodeling and repair of DNA double-strand breaks. J. Mol. Histol. 37:261–269.

    PubMed  CAS  Google Scholar 

  • Wood, R.D. (1999). DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 81:39–44.

    PubMed  CAS  Google Scholar 

  • Wu, S., Shi, Y., Mulligan, P., et al. (2007). A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Mol. Biol. 14:1165–1172.

    PubMed  CAS  Google Scholar 

  • Wyatt, H.R., Liaw, H., Green, G.R., et al. (2003). Multiple roles for Saccharomyces cerevisiae histone H2A in telomere position effect, Spt phenotypes and double-strand-break repair. Genetics 164:47–64.

    PubMed  CAS  Google Scholar 

  • Wysocki, R., Javaheri, A., Allard, S., et al. (2005). Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25:8430–8443.

    PubMed  CAS  Google Scholar 

  • Yang, X.J. (2004). The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32:959–976.

    PubMed  CAS  Google Scholar 

  • You, J.S., Wang, M., Lee, S.H.. (2003). Biochemical analysis of the damage recognition process in nucleotide excision repair. J. Biol. Chem. 278:7476–7485.

    PubMed  CAS  Google Scholar 

  • You, Z., Chahwan, C., Bailis, J., et al. (2005). ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25:5363–5379.

    PubMed  CAS  Google Scholar 

  • Yu,Y., Teng, Y., Liu, H., et al. (2005). UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc. Natl. Acad. Sci. USA. 102:8650–8655.

    PubMed  CAS  Google Scholar 

  • Ziv, Y., Bielopolski, D., Galanty, Y., et al. (2006). Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 8:870–876.

    PubMed  CAS  Google Scholar 

  • Zou, L., and Elledge, S.J. (2003). Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–1548.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank to Drs Anupam Paliwal, Stoyno Stoynov, and Boyka Anachkova for critical reading of the manuscript. A.G. is supported by a Special Training Fellowship from the International Agency for Research on Cancer (IARC), Lyon, France. Work in our laboratory is supported by the International Agency for Research on Cancer (IARC), Lyon (France), and grants from National Institute of Health/National Cancer Institute, USA, the Association pour la Recherche sur le Cancer (ARC), France, la Ligue Nationale (Française) contre le Cancer (France), Institut National du Cancer, (France), Swiss Bridge Award, and Agence Nationale de Recherhe Contre le Sida et Hépatites Virales (ANRS, France) (to Z.H.).

Author information

Authors and Affiliations

  1. Epigenetics Group, International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69008, Lyon, France

    Zdenko Herceg

Authors
  1. Anastas Gospodinov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zdenko Herceg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zdenko Herceg .

Editor information

Editors and Affiliations

  1. Depto. Quimica Inorganica, Universidad Murcia, Murcia, Spain

    Cecilio J. Vidal

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Gospodinov, A., Herceg, Z. (2011). Chromatin: The Entry to and Exit from DNA Repair. In: Vidal, C. (eds) Post-Translational Modifications in Health and Disease. Protein Reviews, vol 13. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6382-6_16

Download citation

Publish with us

Policies and ethics

Search

Navigation