Co-operation of BRCA1 and POH1 relieves the barriers posed by 53BP1 and RAP80 to resection

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10298-10311

  Kakarougkas, Andreas ^a   Ismail, Amani ^a   Katsuki, Yoko ^a   Freire, Raimundo ^b   Shibata, Atsushi ^a   Jeggo, Penny A ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b HOSPITAL UNIVERSITARIO DE CANARIAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

53BP1 PROTEIN; BRCA1 A COMPLEX SUBUNIT; BRCA1 PROTEIN; DEUBIQUITINASE; LYS 63 SPECIFIC DEUBIQUITINASE; MEMBRANE PROTEIN; POH1 PROTEIN; PROTEASOME; RECEPTOR ASSOCIATED PROTEIN 80; REPLICATION FACTOR A; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE G2 PHASE; CONTROLLED STUDY; G2 PHASE CELL CYCLE CHECKPOINT; IMMUNOFLUORESCENCE; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RING FINGER MOTIF; RNA TRANSLATION; UBIQUITINATION;

ANIMALS; BRCA1 PROTEIN; CARRIER PROTEINS; CELLS, CULTURED; G2 PHASE; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; TRANS-ACTIVATORS; UBIQUITIN;

EID: 84890324730     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt802     Document Type: Article

References (33)

1. Mahaney, B.L., Meek, K. and Lees-Miller, S.P. (2009) Repair of ionizing radiation-induced DNA double-strand breaks by nonhomologous end-joining. Biochem. J., 417, 639-650.
2. Petermann, E. and Helleday, T. (2010) Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol., 11, 683-687.
3. Beucher, A., Birraux, J., Tchouandong, L., Barton, O., Shibata, A., Conrad, S., Goodarzi, A.A., Krempler, A., Jeggo, P.A. and Lobrich, M. (2009) ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J., 28, 3413-3427.
4. Shibata, A., Conrad, S., Birraux, J., Geuting, V., Barton, O., Ismail, A., Kakarougkas, A., Meek, K., Taucher-Scholz, G., Lobrich, M. et al. (2011) Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J., 30, 1079-1092.
5. Panier, S. and Durocher, D. (2009) Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair (Amst.), 8, 436-443.
6. Jackson, S.P. and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
7. Acs, K., Luijsterburg, M.S., Ackermann, L., Salomons, F.A., Hoppe, T. and Dantuma, N.P. (2011) The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat. Struct. Mol. Biol., 18, 1345-1350.
8. Mallette, F.A., Mattiroli, F., Cui, G., Young, L.C., Hendzel, M.J., Mer, G., Sixma, T.K. and Richard, S. (2012) RNF8-and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J., 31, 1865-1878.
9. Feng, L., Wang, J. and Chen, J. (2010) The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J. Biol. Chem., 285, 30982-30988.
10. Xie, A., Hartlerode, A., Stucki, M., Odate, S., Puget, N., Kwok, A., Nagaraju, G., Yan, C., Alt, F.W., Chen, J. et al. (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell, 28, 1045-1057.
11. Moynahan, M.E., Chiu, J.W., Koller, B.H. and Jasin, M. (1999) Brca1 controls homology-directed DNA repair. Mol. Cell, 4, 511-518.
12. 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.
13. 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.
14. Bothmer, A., Robbiani, D.F., Di Virgilio, M., Bunting, S.F., Klein, I.A., Feldhahn, N., Barlow, J., Chen, H.T., Bosque, D., Callen, E. et al. (2011) Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol. Cell, 42, 319-329.
15. Chapman, J.R., Sossick, A.J., Boulton, S.J. and Jackson, S.P. (2012) BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair. J. Cell Sci., 125(Pt. 15), 3529-3534.
16. Huen, M.S., Sy, S.M. and Chen, J. (2010) BRCA1 and its x for the maintenance of genome integrity. Nat. Rev. Mol. Cell. Biol, 11, 138-148.
17. Coleman, K.A. and Greenberg, R.A. (2011) The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J. Biol. Chem, 286, 13669-13680.
18. Hu, Y., Scully, R., Sobhian, B., Xie, A., Shestakova, E. and Livingston, D.M. (2011) RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev., 25, 685-700.
19. Sobhian, B., Shao, G., Lilli, D.R., Culhane, A.C., Moreau, L.A., Xia, B., Livingston, D.M. and Greenberg, R.A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science, 316, 1198-1202.
20. Butler, L.R., Densham, R.M., Jia, J., Garvin, A.J., Stone, H.R., Shah, V., Weekes, D., Festy, F., Beesley, J. and Morris, J.R. (2012) The proteosomal de-Ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J., 12, 3918-3934.
21. Pellegrini, L., Yu, D.S., Lo, T., Anand, S., Lee, M., Blundell, T.L. and Venkitaraman, A.R. (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature, 420, 287-293.
22. Chen, L., Nievera, C.J., Lee, A.Y. and Wu, X. (2008) Cell cycledependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem., 283, 7713-7720.
23. Choudhary, S.K. and Li, R. (2002) BRCA1 modulates ionizing radiation-induced nuclear focus formation by the replication protein A p34 subunit. J. Cell. Biochem., 84, 666-674.
24. Schlegel, B.P., Jodelka, F.M. and Nunez, R. (2006) BRCA1 promotes induction of ssDNA by ionizing radiation. Cancer Res., 66, 5181-5189.
25. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M.B., Bartek, J. and Lukas, J. (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol., 173, 195-206.
26. Pei, H., Zhang, L., Luo, K., Qin, Y., Chesi, M., Fei, F., Bergsagel, P.L., Wang, L., You, Z. and Lou, Z. (2011) MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature, 470, 124-128.
27. Shakya, R., Reid, L.J., Reczek, C.R., Cole, F., Egli, D., Lin, C.S., deRooij, D.G., Hirsch, S., Ravi, K., Hicks, J.B. et al. (2011) BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science, 334, 525-528.
28. Noon, A.T. and Goodarzi, A.A. (2011) 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA Repair, 10, 1071-1076.
29. Botuyan, M.V., Lee, J., Ward, I.M., Kim, J.E., Thompson, J.R., Chen, J. and Mer, G. (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell, 127, 1361-1373.
30. 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.
31. Pinato, S., Gatti, M., Scandiuzzi, C., Confalonieri, S. and Penengo, L. (2011) UMI, a novel RNF168 ubiquitin binding domain involved in the DNA damage signaling pathway. Mol. Cell Biol., 31, 118-126.
32. 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.
33. 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.