BRG1 promotes the repair of DNA double-strand breaks by facilitating the replacement of RPA with RAD51

Journal of Cell Science

Volumn 128, Issue 2, 2015, Pages 317-330

  Qi, Wenjing ^a   Wang, Ruoxi ^a   Chen, Hongyu ^a   Wang, Xiaolin ^a   Xiao, Ting ^a   Boldogh, Istvan ^b   Ba, Xueqing ^a   Han, Liping ^c   Zeng, Xianlu ^a  

^a NORTHEAST NORMAL UNIVERSITY   (China)

^b University of Texas Medical Branch School of Medicine   (United States)

^c CHANGCHUN NORMAL UNIVERSITY   (China)

Author keywords

BRG1; DNA double strand break; Homologous recombination; RAD51; RAD52

Indexed keywords

BRG1 PROTEIN; DOUBLE STRANDED DNA; RAD51 PROTEIN; RAD52 PROTEIN; REPLICATION FACTOR A; SINGLE STRANDED DNA; DNA HELICASE; ETOPOSIDE; NUCLEAR PROTEIN; RAD52 PROTEIN, HUMAN; RPA1 PROTEIN, HUMAN; SMARCA4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DNA STRAND; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; LETHALITY; MAMMAL CELL; PRIORITY JOURNAL; RECOMBINATION REPAIR; BIOSYNTHESIS; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; GENETICS; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION;

MAMMALIA;

CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA END-JOINING REPAIR; DNA HELICASES; DNA, SINGLE-STRANDED; ETOPOSIDE; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMANS; NUCLEAR PROTEINS; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; REPLICATION PROTEIN A; TRANSCRIPTION FACTORS;

EID: 84921368168     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.159103     Document Type: Article

References (57)

1. Agger, K., Santoni-Rugiu, E., Holmberg, C., Karlström, O. and Helin, K. (2005). Conditional E2F1 activation in transgenic mice causes testicular atrophy and dysplasia mimicking human CIS. Oncogene 24, 780-789.
2. Bennardo, N., Cheng, A., Huang, N. and Stark, J. M. (2008). Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4, e1000110.
3. Bultman, S., Gebuhr, T., Yee, D., La Mantia, C., Nicholson, J., Gilliam, A., Randazzo, F., Metzger, D., Chambon, P., Crabtree, G. et al. (2000). A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295.
4. Chai, B., Huang, J., Cairns, B. R. and Laurent, B. C. (2005). Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656-1661.
5. Chen, X., Cui, D., Papusha, A., Zhang, X., Chu, C. D., Tang, J., Chen, K., Pan, and Ira, G. (2012). The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489, 576-580.
6. Costelloe, T., Louge, R., Tomimatsu, N., Mukherjee, B., Martini, E., Khadaroo, B., Dubois, K., Wiegant, W. W., Thierry, A., Burma, S. et al. (2012). The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489, 581-584.
7. Cruz, L. A., Guecheva, T. N., Bonato, D. and Henriques, J. A. (2012). Relationships between chromatin remodeling and DNA damage repair induced by 8-methoxypsoralen and UVA in yeast Saccharomyces cerevisiae. Genet. Mol. Biol. 35 Suppl. 4, 1052-1059.
8. Eapen, V. V., Sugawara, N., Tsabar, M., Wu, W. H. and Haber, J. E. (2012). The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol. Cell. Biol. 32, 4727-4740.
9. Falck, J., Coates, J. and Jackson, S. P. (2005). Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434, 605-611.
10. Feng, Z., Scott, S. P., Bussen, W., Sharma, G. G., Guo, G., Pandita, T. K. and Powell, S. N. (2011). Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci. USA 108, 686-691.
11. Franken, N. A., Rodermond, H. M., Stap, J., Haveman, J. and van Bree, C. (2006). Clonogenic assay of cells in vitro. Nat. Protoc. 1, 2315-2319.
12. Helfricht, A., Wiegant, W. W., Thijssen, P. E., Vertegaal, A. C., Luijsterburg, M. S. and van Attikum, H. (2013). Remodeling and spacing factor 1 (RSF1) deposits centromere proteins at DNA double-strand breaks to promote non-homologous end-joining. Cell Cycle 12, 3070-3082.
13. Iacovoni, J. S., Caron, P., Lassadi, I., Nicolas, E., Massip, L., Trouche, D. and Legube, G. (2010). High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29, 1446-1457.
14. Johnson, R. D. and Jasin, M. (2000). Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19, 3398-3407.
15. Khanna, K. K. and Jackson, S. P. (2001). DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27, 247-254.
16. 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.
17. Kwon, S. J., Park, J. H., Park, E. J., Lee, S. A., Lee, H. S., Kang, S. W. and Kwon, J. (2014). ATM-mediated phosphorylation of the chromatin remodeling enzyme BRG1 modulates DNA double-strand break repair. Oncogene.
18. Lee, H. S., Park, J. H., Kim, S. J., Kwon, S. J. and Kwon, J. (2010). A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. EMBO J. 29, 1434-1445.
19. Lim, D. S., Vogel, H., Willerford, D. M., Sands, A. T., Platt, K. A. and Hasty, P. (2000). Analysis of ku80-mutant mice and cells with deficient levels of p53. Mol. Cell. Biol. 20, 3772-3780.
20. Lisby, M., Barlow, J. H., Burgess, R. C. and Rothstein, R. (2004). Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713.
21. Littlewood, T. D., Hancock, D. C., Danielian, P. S., Parker, M. G. and Evan, G. I. (1995). A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23, 1686-1690.
22. Liu, J. and Heyer, W. D. (2011). Who's who in human recombination: BRCA2 and RAD52. Proc. Natl. Acad. Sci. USA 108, 441-442.
23. Liu, J., Doty, T., Gibson, B. and Heyer, W. D. (2010). Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat. Struct. Mol. Biol. 17, 1260-1262.
24. Lok, B. H., Carley, A. C., Tchang, B. and Powell, S. N. (2013). RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination. Oncogene 32, 3552-3558.
25. Martens, J. A. and Winston, F. (2003). Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13, 136-142.
26. Morshead, K. B., Ciccone, D. N., Taverna, S. D., Allis, C. D. and Oettinger, M. A. (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.
27. New, J. H., Sugiyama, T., Zaitseva, E. and Kowalczykowski, S. C. (1998). Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407-410.
28. Nimonkar, A. V., Genschel, J., Kinoshita, E., Polaczek, P., Campbell, J. L., Wyman, C., Modrich, P. and Kowalczykowski, S. C. (2011). BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 25, 350-362.
29. O'Driscoll, M. (2012). Diseases associated with defective responses to DNA damage. Cold Spring Harb. Perspect. Biol. 4, 4.
30. Osley, M. A., Tsukuda, T. and Nickoloff, J. A. (2007). ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 618, 65-80.
31. Park, J. H., Park, E. J., Lee, H. S., Kim, S. J., Hur, S. K., Imbalzano, A. N. and Kwon, J. (2006). Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J. 25, 3986-3997.
32. Patenge, N., Elkin, S. K. and 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.
33. Peng, G., Yim, E. K., Dai, H., Jackson, A. P., Burgt, I., Pan, M. R., Hu, R., Li, K. and Lin, S. Y. (2009). BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat. Cell Biol. 11, 865-872.
34. Peterson, C. L. and Almouzni, G. (2013). Nucleosome dynamics as modular systems that integrate DNA damage and repair. Cold Spring Harb. Perspect. Biol. 5, a012658.
35. Rai, R., Dai, H., Multani, A. S., Li, K., Chin, K., Gray, J., Lahad, J. P., Liang, J., Mills, G. B., Meric-Bernstam, F. et al. (2006). BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 10, 145-157.
36. Ray, A., Mir, S. N., Wani, G., Zhao, Q., Battu, A., Zhu, Q., Wang, Q. E. and Wani, A. A. (2009). Human SNF5/INI1, a component of the human SWI/SNF chromatin remodeling complex, promotes nucleotide excision repair by influencing ATM recruitment and downstream H2AX phosphorylation. Mol. Cell. Biol. 29, 6206-6219.
37. Rich, T., Allen, R. L. and Wyllie, A. H. (2000). Defying death after DNA damage. Nature 407, 777-783.
38. Roberts, C. W. and Orkin, S. H. (2004). The SWI/SNF complex-chromatin and cancer. Nat. Rev. Cancer 4, 133-142.
39. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
40. San Filippo, J., Sung, P. and Klein, H. (2008). Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257.
41. Shinohara, A. and Ogawa, T. (1998). Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391, 404-407.
42. Smith, C. L. and Peterson, C. L. (2004). ATP-dependent chromatin remodeling. Curr. Top. Dev. Biol. 65, 115-148.
43. Sugiyama, T. and Kowalczykowski, S. C. (2002). Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 277, 31663-31672.
44. Sung, P. A., Libura, J. and Richardson, C. (2006). Etoposide and illegitimate DNA double-strand break repair in the generation of MLL translocations: new insights and new questions. DNA Repair (Amst.) 5, 1109-1118.
45. Symington, L. S. (2002). Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670.
46. Tong, H., Zhao, B., Shi, H., Ba, X., Wang, X., Jiang, Y. and Zeng, X. (2013). c-Abl tyrosine kinase plays a critical role in b2 integrin-dependent neutrophil migration by regulating Vav1 activity. J. Leukoc. Biol. 93, 611-622.
47. Tyteca, S., Vandromme, M., Legube, G., Chevillard-Briet, M. and Trouche, D. (2006). Tip60 and p400 are both required for UV-induced apoptosis but play antagonistic roles in cell cycle progression. EMBO J. 25, 1680-1689.
48. van Attikum, H. and Gasser, S. M. (2009). Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19, 207-217.
49. van Gent, D. C., Hoeijmakers, J. H. and Kanaar, R. (2001). Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2, 196-206.
50. Wang, X. and Haber, J. E. (2004). Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2, E21.
51. Weinstock, D. M., Nakanishi, K., Helgadottir, H. R. and Jasin, M. (2006). Assaying double-strand break repair pathway choice in mammalian cells using a targeted endonuclease or the RAG recombinase. Methods Enzymol. 409, 524-540.
52. Wolner, B., van Komen, S., Sung, P. and Peterson, C. L. (2003). Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12, 221-232.
53. Wong, A. K., Shanahan, F., Chen, Y., Lian, L., Ha, P., Hendricks, K., Ghaffari, S., Iliev, D., Penn, B., Woodland, A. M. et al. (2000). BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res. 60, 6171-6177.
54. Wray, J., Liu, J., Nickoloff, J. A. and Shen, Z. (2008). Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Res. 68, 2699-2707.
55. Xu, Y., Sun, Y., Jiang, X., Ayrapetov, M. K., Moskwa, P., Yang, S., Weinstock, D. M. and Price, B. D. (2010). The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J. Cell Biol. 191, 31-43.
56. Yun, M. H. and Hiom, K. (2009). CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 459, 460-463.
57. Zhang, J., Ma, Z., Treszezamsky, A. and Powell, S. N. (2005). MDC1 interacts with Rad51 and facilitates homologous recombination. Nat. Struct. Mol. Biol. 12, 902-909.