NuMA promotes homologous recombination repair by regulating the accumulation of the ISWI ATPase SNF2h at DNA breaks

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6365-6379

  Vidi, Pierre Alexandre ^a   Liu, Jing ^b   Salles, Daniela ^c   Jayaraman, Swaathi ^a   Dorfman, George ^d   Gray, Matthew ^a   Abad, Patricia ^a   Moghe, Prabhas V ^d   Irudayaraj, Joseph M ^b,e   Wiesmüller, Lisa ^c   Lelièvre, Sophie A ^a,e  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF ULM   (Germany)

^d RUTGERS UNIVERSITY   (United States)

^e Purdue University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; NUCLEAR PROTEIN; NUMA PROTEIN; SCAFFOLD PROTEIN; SNF2H PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA CLEAVAGE; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME REGULATION; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECOMBINATION REPAIR; SENSITIVITY ANALYSIS;

ADENOSINE TRIPHOSPHATASES; ANTIGENS, NUCLEAR; CELL LINE; CELL LINE, TUMOR; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; HISTONES; HUMANS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; RECOMBINATIONAL DNA REPAIR;

EID: 84903162148     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku296     Document Type: Article

References (65)

1. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
2. Misteli, T. and Soutoglou, E. (2009) The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat. Rev. Mol. Cell. Biol., 10, 243-254.
3. Morrison, A.J. and Shen, X. (2009) Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell. Biol., 10, 373-384.
4. Seeber, A., Hauer, M. and Gasser, S.M. (2013) Nucleosome remodelers in double-strand break repair. Curr. Opin. Genet. Dev., 23, 174-184.
5. Erdel, F., Schubert, T., Marth, C., Langst, G. and Rippe, K. (2010) Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl. Acad. Sci. U.S.A., 107, 19873-19878.
6. Lan, L., Ui, A., Nakajima, S., Hatakeyama, K., Hoshi, M., Watanabe, R., Janicki, S.M., Ogiwara, H., Kohno, T., Kanno, S. et al. (2010) The ACF1 complex is required for DNA double-strand break repair in human cells. Mol. Cell, 40, 976-987.
7. Nakamura, K., Kato, A., Kobayashi, J., Yanagihara, H., Sakamoto, S., Oliveira, D.V., Shimada, M., Tauchi, H., Suzuki, H., Tashiro, S. et al. (2011) Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell, 41, 515-528.
8. Liu, B., Wang, J., Chan, K.M., Tjia, W.M., Deng, W., Guan, X., Huang, J.D., Li, K.M., Chau, P.Y., Chen, D.J. et al. (2005) Genomic instability in laminopathy-based premature aging. Nat. Med., 11, 780-785.
9. Liu, Y., Wang, Y., Rusinol, A.E., Sinensky, M.S., Liu, J., Shell, S.M. and Zou, Y. (2008) Involvement of xeroderma pigmentosum group A (XPA) in progeria arising from defective maturation of prelamin A. FASEB J., 22, 603-611.
10. Redwood, A.B., Perkins, S.M., Vanderwaal, R.P., Feng, Z., Biehl, K.J., Gonzalez-Suarez, I., Morgado-Palacin, L., Shi, W., Sage, J., Roti-Roti, J.L. et al. (2011) A dual role for A-type lamins in DNA double-strand break repair. Cell Cycle, 10, 2549-2560.
11. Zhang, P., Herbig, U., Coffman, F. and Lambert, M.W. (2013) Non-erythroid alpha spectrin prevents telomere dysfunction after DNA interstrand cross-link damage. Nucleic Acids Res., 41, 5321-5340.
12. Radulescu, A.E. and Cleveland, D.W. (2010) NuMA after 30 years: the matrix revisited. Trends Cell Biol., 20, 214-222.
13. Yang, C.H., Lambie, E.J. and Snyder, M. (1992) NuMA: an unusually long coiled-coil related protein in the mammalian nucleus. J. Cell Biol., 116, 1303-1317.
14. Stokes, M.P., Rush, J., Macneill, J., Ren, J.M., Sprott, K., Nardone, J., Yang, V., Beausoleil, S.A., Gygi, S.P., Livingstone, M. et al. (2007) Profiling of UV-induced ATM/ATR signaling pathways. Proc. Natl. Acad. Sci. U.S.A., 104, 19855-19860.
15. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R. 3rd, Hurov, K.E., Luo, J., Bakalarski, C.E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.
16. Bennetzen, M.V., Larsen, D.H., Bunkenborg, J., Bartek, J., Lukas, J. and Andersen, J.S. (2010) Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol. Cell. Proteomics, 9, 1314-1323.
17. Beli, P., Lukashchuk, N., Wagner, S.A., Weinert, B.T., Olsen, J.V., Baskcomb, L., Mann, M., Jackson, S.P. and Choudhary, C. (2012) Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol. Cell, 46, 212-225.
18. Vidi, P.A., Chandramouly, G., Gray, M., Wang, L., Liu, E., Kim, J.J., Roukos, V., Bissell, M.J., Moghe, P.V. and Lelievre, S.A. (2012) Interconnected contribution of tissue morphogenesis and the nuclear protein NuMA to the DNA damage response. J. Cell Sci., 125, 350-361.
19. Lelìevre, S.A., Weaver, V.M., Nickerson, J.A., Larabell, C.A., Bhaumik, A., Petersen, O.W. and Bissell, M.J. (1998) Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proc. Natl. Acad. Sci. U.S.A., 95, 14711-14716.
20. Chandramouly, G., Abad, P.C., Knowles, D.W. and Lelìevre, S.A. (2007) The control of tissue architecture over nuclear organization is crucial for epithelial cell fate. J. Cell Sci., 120, 1596-1606.
21. Keimling, M., Volcic, M., Csernok, A., Wieland, B., Dork, T. and Wiesmuller, L. (2011) Functional characterization connects individual patient mutations in ataxia telangiectasia mutated (ATM) with dysfunction of specific DNA double-strand break-repair signaling pathways. FASEB J., 25, 3849-3860.
22. Volcic, M., Karl, S., Baumann, B., Salles, D., Daniel, P., Fulda, S. and Wiesmuller, L. (2012) NF-kappaB regulates DNA double-strand break repair in conjunction with BRCA1-CtIP complexes. Nucleic Acids Res., 40, 181-195.
23. Abad, P.C., Lewis, J., Mian, I.S., Knowles, D.W., Sturgis, J., Badve, S., Xie, J. and Lelìevre, S.A. (2007) NuMA influences higher order chromatin organization in human mammary epithelium. Mol. Biol. Cell, 18, 348-361.
24. Nickerson, J.A., Krockmalnic, G., Wan, K.M. and Penman, S. (1997) The nuclear matrix revealed by eluting chromatin from a cross-linked nucleus. Proc. Natl. Acad. Sci. U.S.A., 94, 4446-4450.
25. Huyen, Y., Zgheib, O., Ditullio, R.A. Jr, Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S. and Halazonetis, T.D. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature, 432, 406-411.
26. Sartori, A.A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
27. Merdes, A., Heald, R., Samejima, K., Earnshaw, W.C. and Cleveland, D.W. (2000) Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol., 149, 851-862.
28. Leonhardt, H., Rahn, H.P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D. and Cardoso, M.C. (2000) Dynamics of DNA replication factories in living cells. J. Cell Biol., 149, 271-280.
29. Lambert, S. and Lopez, B.S. (2000) Characterization of mammalian RAD51 double strand break repair using non-lethal dominant-negative forms. EMBO J., 19, 3090-3099.
30. Akyuz, N., Boehden, G.S., Susse, S., Rimek, A., Preuss, U., Scheidtmann, K.H. and Wiesmuller, L. (2002) DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol. Cell. Biol., 22, 6306-6317.
31. Zink, D., Mayr, C., Janz, C. and Wiesmuller, L. (2002) Association of p53 and MSH2 with recombinative repair complexes during S phase. Oncogene, 21, 4788-4800.
32. Treiser, M.D., Yang, E.H., Gordonov, S., Cohen, D.M., Androulakis, I.P., Kohn, J., Chen, C.S. and Moghe, P.V. (2010) Cytoskeleton-based forecasting of stem cell lineage fates. Proc. Natl. Acad. Sci. U.S.A., 107, 610-615.
33. Bozhenok, L., Wade, P.A. and Varga-Weisz, P. (2002) WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. EMBO J., 21, 2231-2241.
34. Xiao, A., Li, H., Shechter, D., Ahn, S.H., Fabrizio, L.A., Erdjument-Bromage, H., Ishibe-Murakami, S., Wang, B., Tempst, P., Hofmann, K. et al. (2009) WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature, 457, 57-62.
35. Goodarzi, A.A., Noon, A.T., Deckbar, D., Ziv, Y., Shiloh, Y., Lobrich, M. and Jeggo, P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31, 167-177.
36. Moyal, L., Lerenthal, Y., Gana-Weisz, M., Mass, G., So, S., Wang, S.Y., Eppink, B., Chung, Y.M., Shalev, G., Shema, E. et al. (2011) Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol. Cell, 41, 529-542.
37. 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.
38. Chang, W., Dynek, J.N. and Smith, S. (2005) NuMA is a major acceptor of poly(ADP-ribosyl)ation by tankyrase 1 in mitosis. Biochem J., 391, 177-184.
39. Boehler, C., Gauthier, L.R., Mortusewicz, O., Biard, D.S., Saliou, J.M., Bresson, A., Sanglier-Cianferani, S., Smith, S., Schreiber, V., Boussin, F. et al. (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl. Acad. Sci. U.S.A., 108, 2783-2788.
40. Rulten, S.L., Fisher, A.E., Robert, I., Zuma, M.C., Rouleau, M., Ju, L., Poirier, G., Reina-San-Martin, B. and Caldecott, K.W. (2013) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell, 41, 33-45.
41. Mueller, A.C., Sun, D. and Dutta, A. (2013) The miR-99 family regulates the DNA damage response through its target SNF2H. Oncogene, 32, 1164-1172.
42. Smeenk, G., Wiegant, W.W., Marteijn, J.A., Luijsterburg, M.S., Sroczynski, N., Costelloe, T., Romeijn, R.J., Pastink, A., Mailand, N., Vermeulen, W. et al. (2013) Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J. Cell Sci., 126, 889-903.
43. Toiber, D., Erdel, F., Bouazoune, K., Silberman, D.M., Zhong, L., Mulligan, P., Sebastian, C., Cosentino, C., Martinez-Pastor, B., Giacosa, S. et al. (2013) SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Mol. Cell, 51, 454-468.
44. 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.
45. Escribano-Diaz, C., Orthwein, A., Fradet-Turcotte, A., Xing, M., Young, J.T., Tkac, J., Cook, M.A., Rosebrock, A.P., Munro, M., Canny, M.D. et al. (2013) A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell, 49, 872-883.
46. Chapman, J.R., Barral, P., Vannier, J.B., Borel, V., Steger, M., Tomas-Loba, A., Sartori, A.A., Adams, I.R., Batista, F.D. and Boulton, S.J. (2013) RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell, 49, 858-871.
47. van Attikum, H. and Gasser, S.M. (2009) Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol., 19, 207-217.
48. Braun, S. and Madhani, H.D. (2012) Shaping the landscape: mechanistic consequences of ubiquitin modification of chromatin. EMBO Rep., 13, 619-630.
49. Hinz, J.M. (2010) Role of homologous recombination in DNA interstrand crosslink repair. Environ. Mol. Mutagen., 51, 582-603.
50. Costes, S.V., Chiolo, I., Pluth, J.M., Barcellos-Hoff, M.H. and Jakob, B. (2010) Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat. Res., 704, 78-87.
51. Soria, G., Polo, S.E. and Almouzni, G. (2012) Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell, 46, 722-734.
52. Jungmichel, S., Rosenthal, F., Altmeyer, M., Lukas, J., Hottiger, M.O. and Nielsen, M.L. (2013) Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol. Cell, 52, 272-285.
53. Chang, P., Coughlin, M. and Mitchison, T.J. (2009) Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly. Mol. Biol. Cell, 20, 4575-4585.
54. Santos-Rosa, H., Schneider, R., Bernstein, B.E., Karabetsou, N., Morillon, A., Weise, C., Schreiber, S.L., Mellor, J. and Kouzarides, T. (2003) Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol. Cell, 12, 1325-1332.
55. Faucher, D. and Wellinger, R.J. (2010) Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway. PLoS Genet., 6, e1001082.
56. Poot, R.A., Bozhenok, L., van den Berg, D.L., Steffensen, S., Ferreira, F., Grimaldi, M., Gilbert, N., Ferreira, J. and Varga-Weisz, P.D. (2004) The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat. Cell Biol., 6, 1236-1244.
57. 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.
58. Min, S., Jo, S., Lee, H.S., Chae, S., Lee, J.S., Ji, J.H. and Cho, H. (2013) ATM-dependent chromatin remodeler Rsf-1 facilitates DNA damage checkpoints and homologous recombination repair. Cell Cycle, 13, 666-677.
59. Chou, D.M., Adamson, B., Dephoure, N.E., Tan, X., Nottke, A.C., Hurov, K.E., Gygi, S.P., Colaiacovo, M.P. and Elledge, S.J. (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. U.S.A., 107, 18475-18480.
60. Collins, N., Poot, R.A., Kukimoto, I., Garcia-Jimenez, C., Dellaire, G. and Varga-Weisz, P.D. (2002) An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat. Genet., 32, 627-632.
61. Xu, R., Spencer, V.A. and Bissell, M.J. (2007) Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors. J. Biol. Chem., 282, 14992-14999.
62. Xu, R., Nelson, C.M., Muschler, J.L., Veiseh, M., Vonderhaar, B.K. and Bissell, M.J. (2009) Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol., 184, 57-66.
63. Bruning-Richardson, A., Bond, J., Alsiary, R., Richardson, J., Cairns, D.A., McCormac, L., Hutson, R., Burns, P.A., Wilkinson, N., Hall, G.D. et al. (2012) NuMA overexpression in epithelial ovarian cancer. PLoS One, 7, e38945.
64. Knowles, D.W., Sudar, D., Bator-Kelly, C., Bissell, M.J. and Lelìevre, S.A. (2006) Automated local bright feature image analysis of nuclear protein distribution identifies changes in tissue phenotype. Proc. Natl. Acad. Sci. U.S.A., 103, 4445-4450.
65. Weaver, V.M., Lelìevre, S.A., Lakins, J.N., Chrenek, M.A., Jones, J.C., Giancotti, F., Werb, Z. and Bissell, M.J. (2002) beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell, 2, 205-216.