Mammalian ino80 mediates double-strand break repair through its role in DNA end strand resection

Molecular and Cellular Biology

Volumn 31, Issue 23, 2011, Pages 4735-4745

  Gospodinov, Anastas ^a,d   Vaissiere, Thomas ^a   Krastev, Dragomir B ^b   Legube, Gaëlle ^c   Anachkova, Boyka ^d   Herceg, Zdenko ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d INSTITUTE OF MOLECULAR BIOLOGY   (Bulgaria)

Author keywords

[No Author keywords available]

Indexed keywords

REPLICATION FACTOR A;

ANIMAL EXPERIMENT; ARTICLE; CELL REGENERATION; COMET ASSAY; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; IMMUNOFLUORESCENCE TEST; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL LINE; CHROMATIN; COMET ASSAY; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA, SINGLE-STRANDED; EMBRYONIC STEM CELLS; GENE KNOCKDOWN TECHNIQUES; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICROFILAMENT PROTEINS; PHOSPHORYLATION; REPLICATION PROTEIN A; RNA INTERFERENCE;

EID: 83255185774     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06182-11     Document Type: Article

References (48)

1. Cai, Y., et al. 2007. YY1 functions with INO80 to activate transcription. Nat. Struct. Mol. Biol. 14:872-874.
2. Cejka, P., et al. 2010. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467:112-116.
3. Chen, L., et al. 2011. Subunit organization of the human INO80 chromatin remodeling complex: an evolutionarily conserved core complex catalyzes ATP-dependent nucleosome remodeling. J. Biol. Chem. 286:11283-11289.
4. Clevers, H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469-480.
5. Falbo, K. B., et al. 2009. Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat. Struct. Mol. Biol. 16:1167-1172.
6. Fazzio, T. G., J. T. Huff, and B. Panning. 2008. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134:162-174.
7. FitzGerald, J. E., M. Grenon, and N. F. Lowndes. 2009. 53BP1: function and mechanisms of focal recruitment. Biochem. Soc. Trans. 37:897-904.
8. Fritsch, O., G. Benvenuto, C. Bowler, J. Molinier, and B. Hohn. 2004. The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16:479-485.
9. Gospodinov, A., I. Tsaneva, and B. Anachkova. 2009. RAD51 foci formation in response to DNA damage is modulated by TIP49. Int. J. Biochem. Cell Biol. 41:925-933.
10. Hoeijmakers, J. H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411:366-374.
11. Jin, J., et al. 2005. A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J. Biol. Chem. 280:41207-41212.
12. Kashiwaba, S., et al. 2010. The mammalian INO80 complex is recruited to DNA damage sites in an ARP8 dependent manner. Biochem. Biophys. Res. Commun. 402:619-625.
13. Kittler, R., A. K. Heninger, K. Franke, B. Habermann, and F. Buchholz. 2005. Production of endoribonuclease-prepared short interfering RNAs for gene silencing in mammalian cells. Nat. Methods 2:779-784.
14. Kittler, R., et al. 2007. Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies. Nat. Methods 4:337-344.
15. Loizou, J. I., et al. 2006. Epigenetic information in chromatin: the code of entry for DNA repair. Cell Cycle 5:696-701.
16. McArt, D. G., G. McKerr, C. V. Howard, K. Saetzler, and G. R. Wasson. 2009. Modelling the comet assay. Biochem. Soc. Trans. 37:914-917.
17. Mendez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612.
18. Miller, K. M., et al. 2010. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol. 17:1144-1151.
19. Mimitou, E. P., and L. S. Symington. 2009. DNA end resection: many nucleases make light work. DNA Repair (Amst.) 8:983-995.
20. Morrison, A. J., et al. 2004. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767-775.
21. Murr, R., 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.
22. Olive, P. L., J. P. Banath, and R. E. Durand. 1990. Heterogeneity in radiation- induced DNA damage and repair in tumor and normal cells measured using the "comet" assay. Radiat. Res. 122:86-94.
23. Papamichos-Chronakis, M., J. E. Krebs, and C. L. Peterson. 2006. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20:2437-2449.
24. Papamichos-Chronakis, M., and C. L. Peterson. 2008. The Ino80 chromatinremodeling enzyme regulates replisome function and stability. Nat. Struct. Mol. Biol. 15:338-345.
25. Park, E. J., S. K. Hur, and J. Kwon. 2010. Human INO80 chromatinremodelling complex contributes to DNA double-strand break repair via the expression of Rad54B and XRCC3 genes. Biochem. J. 431:179-187.
26. Pei, H., et al. 2011. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470:124-128.
27. Pierce, A. J., P. Hu, M. Han, N. Ellis, and M. Jasin. 2001. Ku DNA endbinding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15:3237-3242.
28. Polakis, P. 2000. Wnt signaling and cancer. Genes Dev. 14:1837-1851.
29. Raderschall, E., E. I. Golub, and T. Haaf. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. U. S. A. 96:1921-1926.
30. Rappold, I., K. Iwabuchi, T. Date, and J. Chen. 2001. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153:613-620.
31. Rogakou, E. P., C. Boon, C. Redon, and W. M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-916.
32. Sanders, S. L., et al. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614.
33. Schotta, G., 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.
34. Schultz, L. B., N. H. Chehab, A. Malikzay, and T. D. Halazonetis. 2000. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151:1381-1390.
35. Shen, X., R. Ranallo, E. Choi, and C. Wu. 2003. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12:147-155.
36. Shimada, K., et al. 2008. Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr. Biol. 18:566-575.
37. Sonoda, E., H. Hochegger, A. Saberi, Y. Taniguchi, and S. Takeda. 2006. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5:1021-1029.
38. Takata, M., et al. 1998. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:5497-5508.
39. Tardat, M., R. Murr, Z. Herceg, C. Sardet, and E. Julien. 2007. PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol. 179:1413-1426.
40. Tsukuda, T., A. B. Fleming, J. A. Nickoloff, and M. A. Osley. 2005. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379-383.
41. Tsukuda, T., et al. 2009. INO80-dependent chromatin remodeling regulates early and late stages of mitotic homologous recombination. DNA Repair (Amst.) 8:360-369.
42. van Attikum, H., O. Fritsch, and S. M. Gasser. 2007. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26:4113-4125.
43. van Attikum, H., O. Fritsch, B. Hohn, and S. M. Gasser. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777-788.
44. West, S. C. 2003. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4:435-445.
45. Wu, S., et al. 2007. A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Mol. Biol. 14:1165-1172.
46. Wyman, C., and R. Kanaar. 2006. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40:363-383.
47. Xu, Y., et al. 2010. The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J. Cell Biol. 191:31-43.
48. Yang, D., et al. 2002. Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 99:9942-9947.