DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin

Nucleic Acids Research

Volumn 39, Issue 15, 2011, Pages 6489-6499

  Jakob, Burkhard ^a   Splinter, Jörn ^a   Conrad, Sandro ^b   Voss, Kay Obbe ^a   Zink, Daniele ^c   Durante, Marco ^a,b   Löbrich, Markus ^b   Taucher Scholz, Gisela ^a  

^a GSI HELMHOLTZZENTRUM FÜR SCHWERIONENFORSCHUNG GMBH   (Germany)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; GREEN FLUORESCENT PROTEIN; HISTONE H2AX; XRCC1 PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; GAMMA H2AX PROTEIN, MOUSE; GAMMA-H2AX PROTEIN, MOUSE; H2AFX PROTEIN, HUMAN; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HISTONE; NONHISTONE PROTEIN; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

ANIMAL CELL; ARTICLE; CHROMATIN; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; EMBRYO; EUCHROMATIN; FIBROBLAST; HETEROCHROMATIN; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IRRADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; DNA REPAIR; HELA CELL; KINETICS; METABOLISM; PHOSPHORYLATION;

MURINAE;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; EUCHROMATIN; HELA CELLS; HETEROCHROMATIN; HISTONES; HUMANS; KINETICS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 79961207835     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr230     Document Type: Article

References (36)

1. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J. et al. (2002) Genomic instability in mice lacking histone H2AX. Science, 296, 922-927. (Pubitemid 34464900)
2. Bassing, C.H., Chua, K.F., Sekiguchi, J., Suh, H., Whitlow, S.R., Fleming, J.C., Monroe, B.C., Ciccone, D.N., Yan, C., Vlasakova, K. et al. (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA, 99, 8173-8178. (Pubitemid 34651025)
3. Burma, S., Chen, B.P., Murphy, M., Kurimasa, A. and Chen, D.J. (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 276, 42462-42467.
4. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Löbrich, M. and Jeggo, P.A. (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res., 64, 2390-2396. (Pubitemid 38523891)
5. Rogakou, E.P., Boon, C., Redon, C. and Bonner, W.M. (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol., 146, 905-916.
6. Vasireddy, R.S., Karagiannis, T.C. and El-Osta, A. (2010) g-radiation-induced gH2AX formation occurs preferentially in actively transcribed euchromatic loci. Cell. Mol. Life Sci., 67, 291-294.
7. Cowell, I.G., Sunter, N.J., Singh, P.B., Austin, C.A., Durkacz, B.W. and Tilby, M.J. (2007) gH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One, 2, e1057.
8. Goodarzi, A.A., Noon, A.T., Deckbar, D., Ziv, Y., Shiloh, Y., Löbrich, M. and Jeggo, P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31, 167-177. (Pubitemid 352001394)
9. Falk, M., Lukasova, E. and Kozubek, S. (2008) Chromatin structure influences the sensitivity of DNA to g-radiation. Biochim. Biophys. Acta, 1783, 2398-2414.
10. Guenatri, M., Bailly, D., Maison, C. and Almouzni, G. (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol., 166, 493-505. (Pubitemid 39097169)
11. Noon, A.T., Shibata, A., Rief, N., Löbrich, M., Stewart, G.S., Jeggo, P.A. and Goodarzi, A.A. (2010) 53BP1-dependent robust localized KAP-1 phosphorylation is essential for heterochromatic DNA double-strand break repair. Nat. Cell Biol., 12, 177-184.
12. Kim, J.A., Kruhlak, M., Dotiwala, F., Nussenzweig, A. and Haber, E. (2007) Heterochromatin is refractory to g-H2AX modification in yeast and mammals. J. Cell Biol., 178, 209-218. (Pubitemid 47076458)
13. Goodarzi, A., Jeggo, P. and Lobrich, M. (2010) The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair, 9, 1273-1282.
14. Riballo, E., Kühne, M., Rief, N., Doherty, A., Smith, G.C., Recio, M.J., Reis, C., Dahm, K., Fricke, A., Krempler, A. et al. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell, 16, 715-724. (Pubitemid 39586530)
15. Psonka-Antonczyk, K., Elsässer, T., Gudowska-Nowak, E. and Taucher-Scholz, G. (2009) Distribution of double-strand breaks induced by ionizing radiation at the level of single DNA molecules examined by atomic force microcopy. Radiat. Res., 172, 288-295.
16. Asaithamby, A., Uematsu, N., Chatterjee, A., Story, M.D., Burma, S. and Chen, D.J. (2008) Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat. Res., 169, 437-446. (Pubitemid 351620042)
17. Goodarzi, A.A., Noon, A.T. and Jeggo, P.A. (2009) The impact of heterochromatin on DSB repair. Biochem. Soc. Trans., 37, 569-576.
18. Bancaud, A., Huet, S., Daigle, N., Mozziconacci, J., Beaudouin, J. and Ellenberg, J. (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J., 28, 3785-3798.
19. Jakob, B., Scholz, M. and Taucher-Scholz, G. (2003) Biological imaging of heavy charged-particle tracks. Radiat. Res., 159, 676-684. (Pubitemid 36539248)
20. Heiss, M., Fischer, B.E., Jakob, B., Fournier, C., Becker, G. and Taucher-Scholz, G. (2006) Targeted irradiation of mammalian cells using a heavy-ion microprobe. Radiat. Res., 165, 231-239. (Pubitemid 43153136)
21. Jakob, B., Splinter, J. and Taucher-Scholz, G. (2009) Positional stability of damaged chromatin domains along radiation tracks in mammalian cells. Radiat. Res., 171, 405-418.
22. Jakob, B., Rudolph, J.H., Gueven, N., Lavin, M.F. and Taucher-Scholz, G. (2005) Live cell imaging of heavy ion induced radiation responses by beamline microscopy. Radiat. Res., 163, 681-690. (Pubitemid 40734767)
23. Jakob, B., Splinter, J., Durante, M. and Taucher-Scholz, G. (2009) Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc. Natl Acad. Sci. USA, 106, 3172-3177.
24. Tobias, F., Durante, M., Taucher-Scholz, G. and Jakob, B. (2010) Spatiotemporal analysis of DNA repair using charged particle radiation. Mutat. Res., 704, 54-60.
25. Bakkenist, C.J. and Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimmer dissociation. Nature, 421, 499-506. (Pubitemid 36168436)
26. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M.B., Bartek, J. and Lukas, J. (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol., 173, 195-206.
27. Shibata, A., Conrad, S., Birraux, J., Geuting, V., Barton, O., Ismail, A., Kakarougkas, A., Taucher-Scholz, G., Löbrich, M. and Jeggo, P. (2011) Factors determining DNA double strand break repair pathway choice in G2 phase. EMBO J., 30, 1079-1092.
28. Ziv, Y., Bielopolski, D., Galanty, Y., Lukas, C., Taya, Y., Schultz, D.C., Lukas, J., Bekker-Jensen, S., Bartek, J. and Shiloh, Y. (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. (Pubitemid 44151591)
29. Kruhlak, M.J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Müller, W.G., McNally, J.G., Bazett-Jones, D.P. and Nussenzweig, A. (2006) Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol., 172, 823-834.
30. Costes, S.V., Ponomarev, A., Chen, J.L., Nguyen, D., Cucinotta, F.A. and Barcellos-Hoff, M.H. (2007) Image-based modeling reveals dynamic redistribution of DNA damage into nuclear sub-domains. PLoS Comput. Biol., 3, e155.
31. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. and Bonner, W.M. (1998) DNA double-strand breaks induce histone H2AX phosphorylation on serine 139. J. Cell Biol., 273, 5858-5868. (Pubitemid 28124064)
32. Nakamura, A.J., Rao, V.A., Pommier, Y. and Bonner, W.M. (2010) The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle, 9, 389-397.
33. Splinter, J., Jakob, B., Lang, M., Yano, K., Engelhardt, J., Hell, S.W., Chen, D.J., Durante, M. and Taucher-Scholz, G. (2010) Biological dose estimation of UVA laser microirradiation utilizing charged particle-induced protein foci. Mutagenesis, 25, 289-297.
34. Falk, M., Lukasova, E., Gabrielova, B., Ondrej, V. and Kozubek, S. (2007) Chromatin dynamics during DSB repair. Biochim. Biophys. Acta, 1773, 1534-1545. (Pubitemid 47498611)
35. Soutoglou, E., Dorn, J.F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., Danuser, G. and Misteli, T. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol., 9, 675-682. (Pubitemid 47214730)
36. Chiolo, I., Minoda, A., Colmenares, S.U., Polyzos, A., Costes, S.V. and Karpen, G.H. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell, 144, 732-744.