Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM-and KAP-1 dependent pathway

Nature Cell Biology

Volumn 8, Issue 8, 2006, Pages 870-876

  Ziv, Yael ^a   Bielopolski, Dana ^a   Galanty, Yaron ^a   Lukas, Claudia ^b   Taya, Yoichi ^c   Schultz, David C ^d   Lukas, Jiri ^b   Bekker Jensen, Simon ^b   Bartek, Jiri ^b   Shiloh, Yosef ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DOUBLE STRANDED DNA; KRAB ASSOCIATED PROTEIN 1; STEROID RECEPTOR COACTIVATOR 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA STRAND BREAKAGE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION SITE;

BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATIN; DNA DAMAGE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MICROSCOPY, FLUORESCENCE; MUTATION; NUCLEIC ACID SYNTHESIS INHIBITORS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; ZINOSTATIN;

EID: 33746601439     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1446     Document Type: Article

References (36)

1. Bassing, C. H. & Alt, F. W. The cellular response to general and programmed DNA double strand breaks. DNA Repair 3, 781-796 (2004).
2. Shiloh, Y. The ATM-mediated DNA-damage response: Taking shape. Trends Biochem. Sci. doi:10.1016/j.tibs.2006.05.004 (2006).
3. Friedman, J. R. et al. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 10, 2067-2078 (1996).
4. Le Douarin, B. et al. A possible involvement of TIF1α and TIF1β in the epigenetic control of transcription by nuclear receptors. EMBO J 15, 6701-6715 (1996).
5. Shiloh, Y. ATM and related protein kinases: Safeguarding genome integrity. Nature Rev. Cancer 3, 155-168 (2003).
6. Bakkenist, C. J. & Kastan, M. B. Initiating cellular stress responses. Cell 118, 9-17 (2004).
7. Shechter, D., Costanzo, V. & Gautier, J. Regulation of DNA replication by ATR: Signaling in response to DNA intermediates. DNA Repair 3, 901-908 (2004).
8. Shinozaki, T., Nota, A., Taya, Y. & Okamoto, K. Functional role of Mdm2 phosphorylation by ATR in attenuation of p53 nuclear export. Oncogene 22, 8870-8880 (2003).
9. Moosmann, P., Georgiev, O., Le Douarin, B., Bourquin, J. P. & Schaffner, W. Transcriptional repression by RING finger protein TIF1β that interacts with the KRAB repressor domain of KOX1. Nucleic Acids Res. 24, 4859-4867 (1996).
10. Kim, S. S. et al. A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc. Natl Acad. Sci. USA 93, 15299-15304 (1996).
11. Reymond, A. et al. The tripartite motif family identifies cell compartments. EMBO J. 20, 2140-2151 (2001).
12. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. & Rauscher, F. J., 3rd. SETDB1: A novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919-932 (2002).
13. Ayyanathan, K. et al. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: A mammalian cell culture model of gene variegation. Genes Dev. 17, 1855-1869 (2003).
14. Cammas, F., Mark, M., Dolle, P., Chambon, P., Losson, R. Mice lacking the transcriptional corepressor TIF1β are defective in early post implantation development. Development 127, 2955-2963 (2000).
15. Lukas, C., Falck, J., Bartkova, J., Bartek, J. & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biol. 5, 255-260 (2003).
16. Telford, D. J. & Stewart, B. W. Micrococcal nuclease: Its specificity and use for chromatin analysis. Int. J. Biochem. 21, 127-137 (1989).
17. Biton, S. et al. Nuclear ATM mediates the cellular response to DNA double-strand breaks in human neuron-like cells. J. Biol. Chem. 281, 17482-17491 (2006).
18. Lu, Q. & Richardson, B. DNasel hypersensitivity analysis of chromatin structure. Methods Mol. Biol. 287, 77-86 (2004).
19. Gontijo, A. M., Green, C. M. & Almouzni, G. Repairing DNA damage in chromatin. Biochimie 85, 1133-1147 (2003).
20. Verger, A. & Crossley, M. Chromatin modifiers in transcription and DNA repair. Cell Mol. Life Sci. 61, 2154-2162 (2004).
21. Muller, W. G., Walker, D., Hager, G. L. & McNally, J. G. Large-scale chromatin decondensation and recondensation regulated by transcription from a natural promoter. J. Cell Biol. 154, 33-48 (2001).
22. Ye, Q. et al. BRCA1-induced large-scale chromatin unfolding and allele-specific effects of cancer-predisposing mutations. J. Cell Biol. 155, 911-921 (2001).
23. Nye, A. C. et al. Alteration of large-scale chromatin structure by estrogen receptor. Mol. Cell Biol. 22, 3437-3449 (2002).
24. Carpenter, A. E., Memedula, S., Plutz, M. J. & Belmont, A. S. Common effects of acidic activators on large-scale chromatin structure and transcription. Mol. Cell Biol. 25, 958-968 (2005).
25. Carrier, F. et al. Gadd45, a p53-responsive stress protein, modifies DNA accessibility on damaged chromatin. Mol. Cell Biol. 19, 1673-1685 (1999).
26. Rubbi, C. P. & Milner, J. p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J. 22, 975-986 (2003).
27. 60Co γ-rays. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 48, 389-395 (1985).
28. Jaberaboansari, A., Landis, M. R., Wallen, C. A. & Wheeler, K. T. Alterations of neuronal nuclear matrix and chromatin structure after irradiation under aerobic and anoxic conditions. Radiat. Res. 119, 57-72 (1989).
29. 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).
30. 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).
31. Riballo, E. et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to γ-H2AX foci. Mol. Cell 16, 715-724 (2004).
32. Wang, C. et al. MDM2 interaction with nuclear corepressor KAP1 contributes to p53 inactivation. EMBO J. 24, 3279-3290 (2005).
33. Bhoumik, A. et al. ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol. Cell 18, 577-587 (2005).
34. Ljungman, M. & Lane, D. P. Transcription - guarding the genome by sensing DNA damage. Nature Rev. Cancer 4, 727-737 (2004).
35. Birger, Y. et al. Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22, 1665-1675 (2003).
36. Ziv, Y. et al. Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 15, 159-167 (1997).