An RNF168 fragment defective for focal accumulation at DNA damage is proficient for inhibition of homologous recombination in BRCA1 deficient cells

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 7720-7733

  Muñoz, Meilen C ^a   Yanez, Diana A ^a   Stark, Jeremy M ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; HISTONE H2A; HISTONE H2AX; UBIQUITIN PROTEIN LIGASE E3;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; ENZYME INHIBITION; GENE; GENOMIC FRAGMENT; HISTONE UBIQUITINATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; IONIZING RADIATION INDUCED FOCI; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNF168 GENE; TUMOR SUPPRESSOR GENE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BRCA1 PROTEIN; CELL LINE; CHROMOSOME BREAKAGE; CONSERVED SEQUENCE; DEOXYRIBONUCLEASES; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HISTONES; HUMANS; MICE; PROTEIN STRUCTURE, TERTIARY; RECOMBINATIONAL DNA REPAIR; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84904013419     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku421     Document Type: Article

References (55)

1. Stewart, G.S., Stankovic, T., Byrd, P.J., Wechsler, T., Miller, E.S., Huissoon, A., Drayson, M.T., West, S.C., Elledge, S.J., Taylor, A.M. (2007) RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc. Natl. Acad. Sci. U.S.A., 104, 16910-16915.
2. Bohgaki, T., Bohgaki, M., Cardoso, R., Panier, S., Zeegers, D., Li, L., Stewart, G.S., Sanchez, O., Hande, M.P., Durocher, D. et al. (2011) Genomic instability, defective spermatogenesis, immunodeficiency, and cancer in a mouse model of the RIDDLE syndrome. PLoS Genet., 7, e1001381.
3. Devgan, S.S., Sanal, O., Doil, C., Nakamura, K., Nahas, S.A., Pettijohn, K., Bartek, J., Lukas, C., Lukas, J., Gatti, R.A. (2011) Homozygous deficiency of ubiquitin-ligase ring-finger protein RNF168 mimics the radiosensitivity syndrome of ataxia-telangiectasia. Cell Death Differ., 18, 1500-1506.
4. Pinato, S., Scandiuzzi, C., Arnaudo, N., Citterio, E., Gaudino, G., Penengo, L. (2009) RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol. Biol., 10, 55.
5. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D.H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J. et al. (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell, 136, 435-446.
6. Stewart, G.S., Panier, S., Townsend, K., Al-Hakim, A.K., Kolas, N.K., Miller, E.S., Nakada, S., Ylanko, J., Olivarius, S., Mendez, M. et al. (2009) The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell, 136, 420-434.
7. Ward, I.M., Reina-San-Martin, B., Olaru, A., Minn, K., Tamada, K., Lau, J.S., Cascalho, M., Chen, L., Nussenzweig, A., Livak, F. et al. (2004) 53BP1 is required for class switch recombination. J. Cell Biol., 165, 459-464.
8. Munoz, M.C., Laulier, C., Gunn, A., Cheng, A., Robbiani, D.F., Nussenzweig, A., Stark, J.M. (2012) RING finger nuclear factor RNF168 is important for defects in homologous recombination caused by loss of the breast cancer susceptibility factor BRCA1. J. Biol. Chem., 287, 40618-40628.
9. Bunting, S.F., Callen, E., Wong, N., Chen, H.T., Polato, F., Gunn, A., Bothmer, A., Feldhahn, N., Fernandez-Capetillo, O., Cao, L. et al. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell, 141, 243-254.
10. Bouwman, P., Aly, A., Escandell, J.M., Pieterse, M., Bartkova, J., van der Gulden, H., Hiddingh, S., Thanasoula, M., Kulkarni, A., Yang, Q. et al. (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol., 17, 688-695.
11. Mattiroli, F., Vissers, J.H., van Dijk, W.J., Ikpa, P., Citterio, E., Vermeulen, W., Marteijn, J.A., Sixma, T.K. (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell, 150, 1182-1195.
12. Gatti, M., Pinato, S., Maspero, E., Soffientini, P., Polo, S., Penengo, L. (2012) A novel ubiquitin mark at the N-terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle, 11, 2538-2544.
13. Fradet-Turcotte, A., Canny, M.D., Escribano-Diaz, C., Orthwein, A., Leung, C.C., Huang, H., Landry, M.C., Kitevski-LeBlanc, J., Noordermeer, S.M., Sicheri, F. et al. (2013) 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature, 499, 50-54.
14. Huen, M.S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M.B., Chen, J. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell, 131, 901-914.
15. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M. et al. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science, 318, 1637-1640.
16. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., Lukas, J. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell, 131, 887-900.
17. Wang, B., Elledge, S.J. (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A., 104, 20759-20763.
18. Panier, S., Ichijima, Y., Fradet-Turcotte, A., Leung, C.C., Kaustov, L., Arrowsmith, C.H., Durocher, D. (2012) Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell, 47, 383-395.
19. Gudjonsson, T., Altmeyer, M., Savic, V., Toledo, L., Dinant, C., Grofte, M., Bartkova, J., Poulsen, M., Oka, Y., Bekker-Jensen, S. et al. (2012) TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell, 150, 697-709.
20. Panier, S., Durocher, D. (2013) Push back to respond better: regulatory inhibition of the DNA double-strand break response. Nat. Rev. Mol. Cell Biol., 14, 661-672.
21. Evers, B., Helleday, T., Jonkers, J. (2010) Targeting homologous recombination repair defects in cancer. Trends Pharmacol. Sci., 31, 372-380.
22. Moynahan, M.E., Jasin, M. (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis.Nat. Rev. Mol. Cell Biol., 11, 196-207.
23. TCGA. (2011) Integrated genomic analyses of ovarian carcinoma. Nature, 474, 609-615.
24. Kass, E.M., Moynahan, M.E., Jasin, M. (2010) Loss of 53BP1 is a gain for BRCA1 mutant cells. Cancer Cell, 17, 423-425.
25. Pinato, S., Gatti, M., Scandiuzzi, C., Confalonieri, S., Penengo, L. (2011) UMI, a novel RNF168 ubiquitin binding domain involved in the DNA damage signaling pathway. Mol. Cell. Biol., 31, 118-126.
26. Gunn, A., Bennardo, N., Cheng, A., Stark, J.M. (2011) Correct end use during end joining of multiple chromosomal double strand breaks is influenced by repair protein RAD50, DNA-dependent protein kinase DNA-PKcs, and transcription context. J. Biol. Chem., 286, 42470-42482.
27. 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. U.S.A., 99, 8173-8178.
28. Gunn, A., Stark, J.M. (2012) I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods Mol. Biol., 920, 379-391.
29. Lilley, C.E., Chaurushiya, M.S., Boutell, C., Landry, S., Suh, J., Panier, S., Everett, R.D., Stewart, G.S., Durocher, D., Weitzman, M.D. (2010) A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. Embo J., 29, 943-955.
30. Xie, A., Puget, N., Shim, I., Odate, S., Jarzyna, I., Bassing, C.H., Alt, F.W., Scully, R. (2004) Control of sister chromatid recombination by histone H2AX. Mol. Cell, 16, 1017-1025.
31. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
32. Moure, C.M., Gimble, F.S., Quiocho, F.A. (2003) The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity. J. Mol. Biol., 334, 685-695.
33. Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., Zhang, F. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc., 8, 2281-2308.
34. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
35. Pierce, A.J., Johnson, R.D., Thompson, L.H., Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638.
36. Bennardo, N., Cheng, A., Huang, N., Stark, J.M. (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet., 4, e1000110.
37. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
38. Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S., Zhang, Y. et al. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154, 1380-1389.
39. Bennardo, N., Gunn, A., Cheng, A., Hasty, P., Stark, J.M. (2009) Limiting the persistence of a chromosome break diminishes its mutagenic potential. PLoS Genet., 5, e1000683.
40. Stark, J.M., Pierce, A.J., Oh, J., Pastink, A., Jasin, M. (2004) Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol., 24, 9305-9316.
41. Sy, S.M., Jiang, J., Dong, S.S., Lok, G.T., Wu, J., Cai, H., Yeung, E.S., Huang, J., Chen, J., Deng, Y. et al. (2011) Critical roles of ring finger protein RNF8 in replication stress responses. J. Biol. Chem., 286, 22355-22361.
42. Huang, J., Huen, M.S., Kim, H., Leung, C.C., Glover, J.N., Yu, X., Chen, J. (2009) RAD18 transmits DNA damage signalling to elicit homologous recombination repair.Nat. Cell Biol., 11, 592-603.
43. Santos, M.A., Huen, M.S., Jankovic, M., Chen, H.T., Lopez-Contreras, A.J., Klein, I.A., Wong, N., Barbancho, J.L., Fernandez-Capetillo, O., Nussenzweig, M.C. et al. (2010) Class switching and meiotic defects in mice lacking the E3 ubiquitin ligase RNF8. J. Exp. Med., 207, 973-981.
44. Nakada, S., Yonamine, R.M., Matsuo, K. (2012) RNF8 regulates assembly of RAD51 at DNA double-strand breaks in the absence of BRCA1 and 53BP1. Cancer Res., 72, 4974-4983.
45. Kim, H., D'Andrea, A.D. (2012) Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev., 26, 1393-1408.
46. Nakanishi, K., Yang, Y.G., Pierce, A.J., Taniguchi, T., Digweed, M., D'Andrea, A.D., Wang, Z.Q., Jasin, M. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. U.S.A., 102, 1110-1115.
47. Leung, J.W., Agarwal, P., Canny, M.D., Gong, F., Robison, A.D., Finkelstein, I.J., Durocher, D., Miller, K.M. (2014) Nucleosome acidic patch promotes RNF168- and RING1B/BMI1-dependent H2AX and H2A ubiquitination and DNA damage signaling. PLoS Genet., 10, e1004178.
48. Mattiroli, F., Uckelmann, M., Sahtoe, D.D., van Dijk, W.J., Sixma, T.K. (2014) The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nat. Commun., 5, 3291.
49. Kinner, A., Wu, W., Staudt, C., Iliakis, G. (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res., 36, 5678-5694.
50. Soutoglou, E., Misteli, T. (2008) Activation of the cellular DNA damage response in the absence of DNA lesions. Science, 320, 1507-1510.
51. Lukas, J., Lukas, C., Bartek, J. (2011) More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance.Nat. Cell Biol., 13, 1161-1169.
52. Shanbhag, N.M., Rafalska-Metcalf, I.U., Balane-Bolivar, C., Janicki, S.M., Greenberg, R.A. (2010) ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell, 141, 970-981.
53. Ramachandran, S., Chahwan, R., Nepal, R.M., Frieder, D., Panier, S., Roa, S., Zaheen, A., Durocher, D., Scharff, M.D., Martin, A. (2010) The RNF8/RNF168 ubiquitin ligase cascade facilitates class switch recombination. Proc. Natl. Acad. Sci. U.S.A., 107, 809-814.
54. Yan, Z., Guo, R., Paramasivam, M., Shen, W., Ling, C., Fox, D. 3rd, Wang, Y., Oostra, A.B., Kuehl, J., Lee, D.Y. et al. (2012) A ubiquitin-binding protein, FAAP20, links RNF8-mediated ubiquitination to the Fanconi anemia DNA repair network. Mol. Cell, 47, 61-75.
55. Certo, M.T., Gwiazda, K.S., Kuhar, R., Sather, B., Curinga, G., Mandt, T., Brault, M., Lambert, A.R., Baxter, S.K., Jacoby, K. et al. (2012) Coupling endonucleases with DNA end-processing enzymes to drive gene disruption. Nat. Methods, 9, 973-975.