A mechanism for the suppression of homologous recombination in G1 cells

Nature

Volumn 528, Issue 7582, 2015, Pages 422-426

  Orthwein, Alexandre ^a   Noordermeer, Sylvie M ^a   Wilson, Marcus D ^a   Landry, Sébastien ^a   Enchev, Radoslav I ^b   Sherker, Alana ^a,c   Munro, Meagan ^a   Pinder, Jordan ^d   Salsman, Jayme ^d   Dellaire, Graham ^d   Xia, Bing ^e   Peter, Matthias ^b   Durocher, Daniel ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF TORONTO   (Canada)

^d DALHOUSIE UNIVERSITY   (Canada)

^e ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; CULLIN; CULLIN 3; DNA; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PROTEIN; PROTEIN PALB2; PROTEIN RBX1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN, HUMAN; CARRIER PROTEIN; CUL3 PROTEIN, HUMAN; KEAP1 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; PALB2 PROTEIN, HUMAN; PROTEIN BINDING; RAD51 PROTEIN; RAD51 PROTEIN, HUMAN; RBX1 PROTEIN, HUMAN; SIGNAL PEPTIDE; THIOL ESTER HYDROLASE; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE; USP11 PROTEIN, HUMAN;

DNA; PROTEIN; RECOMBINATION;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; HOMOLOGOUS RECOMBINATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; U2OS CELL LINE; UBIQUITINATION; UNSCHEDULED DNA SYNTHESIS; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; CRISPR CAS SYSTEM; DNA DAMAGE; DNA REPAIR; GENE TARGETING; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; BRCA1 PROTEIN; BRCA2 PROTEIN; CARRIER PROTEINS; CELL LINE; CRISPR-CAS SYSTEMS; CULLIN PROTEINS; DNA; DNA DAMAGE; DNA REPAIR; G1 PHASE; G2 PHASE; GENE TARGETING; HOMOLOGOUS RECOMBINATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN BINDING; RAD51 RECOMBINASE; S PHASE; THIOLESTER HYDROLASES; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84950294519     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16142     Document Type: Article

References (39)

1. Jasin, M. & Rothstein, R. Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol. 5, a012740 (2013).
2. Hartlerode, A., Odate, S., Shim, I., Brown, J. & Scully, R. Cell cycle-dependent induction of homologous recombination by a tightly regulated I-SceI fusion protein. PLoS ONE 6, e16501 (2011).
3. Rothkamm, K., Krüger, I., Thompson, L. H. & Löbrich, M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23, 5706-5715 (2003).
4. Panier, S. & Durocher, D. Push back to respond better: regulatory inhibition of the DNA double-strand break response. Nature Rev. Mol. Cell Biol. 14, 661-672 (2013).
5. Ma, J. et al. PALB2 interacts with KEAP1 to promote NRF2 nuclear accumulation and function. Mol. Cell. Biol. 32, 1506-1517 (2012).
6. Genschik, P., Sumara, I. & Lechner, E. The emerging family of CULLIN3-RING ubiquitin ligases (CRL3s): cellular functions and disease implications. EMBO J. 32, 2307-2320 (2013).
7. Roy, R., Chun, J. & Powell, S. N. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nature Rev. Cancer 12, 68-78 (2012).
8. Li, M. L. & Greenberg, R. A. Links between genome integrity and BRCA1 tumor suppression. Trends Biochem. Sci. 37, 418-424 (2012).
9. Park, J. Y., Zhang, F. & Andreassen, P. R. PALB2: the hub of a network of tumor suppressors involved in DNA damage responses. Biochim. Biophys. Acta 1846, 263-275 (2014).
10. Zhang, F. et al. PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr. Biol. 19, 524-529 (2009).
11. Sy, S. M., Huen, M. S. & Chen, J. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc. Natl Acad. Sci. USA 106, 7155-7160 (2009).
12. Simhadri, S. et al. Male fertility defect associated with disrupted BRCA1-PALB2 interaction in mice. J. Biol. Chem. 289, 24617-24629 (2014).
13. Bhattacharyya, A., Ear, U. S., Koller, B. H., Weichselbaum, R. R. & Bishop, D. K. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA crosslinking agent cisplatin. J. Biol. Chem. 275, 23899-23903 (2000).
14. Zhang, F., Bick, G., Park, J. Y. & Andreassen, P. R. MDC1 and RNF8 function in a pathway that directs BRCA1-dependent localization of PALB2 required for homologous recombination. J. Cell Sci. 125, 6049-6057 (2012).
15. Escribano-Díaz, C. et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell 49, 872-883 (2013).
16. Feng, L., Fong, K. W., Wang, J., Wang, W. & Chen, J. RIF1 counteracts BRCA1-mediated end resection during DNA repair. J. Biol. Chem. 288, 11135-11143 (2013).
17. Chapman, J. R. et al. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell 49, 858-871 (2013).
18. Bunting, S. F. et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141, 243-254 (2010).
19. Zimmermann, M., Lottersberger, F., Buonomo, S. B., Sfeir, A. & de Lange, T. 53BP1 regulates DSB repair using Rif1 to control 5′ end resection. Science 339, 700-704 (2013).
20. Tang, J. et al. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nature Struct. Mol. Biol. 20, 317-325 (2013).
21. Taguchi, K., Motohashi, H. & Yamamoto, M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16, 123-140 (2011).
22. Sowa, M. E., Bennett, E. J., Gygi, S. P. & Harper, J. W. Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403 (2009).
23. Schoenfeld, A. R., Apgar, S., Dolios, G., Wang, R. & Aaronson, S. A. BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol. Cell. Biol. 24, 7444-7455 (2004).
24. Wiltshire, T. D. et al. Sensitivity to poly(ADP-ribose) polymerase (PARP) inhibition identifies ubiquitin-specific peptidase 11 (USP11) as a regulator of DNA double-strand break repair. J. Biol. Chem. 285, 14565-14571 (2010).
25. Enchev, R. I., Schulman, B. A. & Peter, M. Protein neddylation: beyond cullin-RING ligases. Nature Rev. Mol. Cell Biol. 16, 30-44 (2015).
26. Yamane, A. et al. RPA accumulation during class switch recombination represents 5′-3′ DNA-end resection during the S-G2/M phase of the cell cycle. Cell Reports 3, 138-147 (2013).
27. Huertas, P. & Jackson, S. P. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 284, 9558-9565 (2009).
28. Pinder, J., Salsman, J. & Dellaire, G. Nuclear domain 'knock-in' screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing. Nucleic Acids Res. 43, 9379-9392 (2015).
29. Fradet-Turcotte, A. et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499, 50-54 (2013).
30. Enchev, R. I., Schreiber, A., Beuron, F. & Morris, E. P. Structural insights into the COP9 signalosome and its common architecture with the 26S proteasome lid and eIF3. Structure 18, 518-527 (2010).
31. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 8, 2281-2308 (2013).
32. Xia, B. et al. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 22, 719-729 (2006).
33. Orthwein, A. et al. Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344, 189-193 (2014).
34. Panier, S. et al. Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47, 383-395 (2012).
35. Juang, Y. C. et al. OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol. Cell 45, 384-397 (2012).
36. Cui, J. et al. Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 329, 1215-1218 (2010).
37. Hendriks, I. A., Schimmel, J., Eifler, K., Olsen, J. V. & Vertegaal, A. C. Ubiquitin-specific protease 11 (USP11) deubiquitinates hybrid small ubiquitin-like modifier (SUMO)-ubiquitin chains to counteract RING finger protein 4 (RNF4). J. Biol. Chem. 290, 15526-15537 (2015).
38. Long, L., Furgason, M. & Yao, T. Generation of nonhydrolyzable ubiquitin-histone mimics. Methods 70, 134-138 (2014).
39. Yin, L., Krantz, B., Russell, N. S., Deshpande, S. & Wilkinson, K. D. Nonhydrolyzable diubiquitin analogues are inhibitors of ubiquitin conjugation and deconjugation. Biochemistry 39, 10001-10010 (2000).