Neddylation inhibits CtIP-mediated resection and regulates DNA double strand break repair pathway choice

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 987-999

  Jimeno, Sonia ^a,b   Fernández Ávila, María Jesús ^a   Cruz García, Andrés ^a,b   Cepeda García, Cristina ^a   Gómez Cabello, Daniel ^a   Huertas, Pablo ^a,b  

^a CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; CARRIER PROTEIN; DNA; NUCLEAR PROTEIN; RBBP8 PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

CELL LINE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; METABOLISM; RECOMBINATION REPAIR;

BRCA1 PROTEIN; CARRIER PROTEINS; CELL LINE; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR; HUMANS; NUCLEAR PROTEINS; RECOMBINATIONAL DNA REPAIR; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

EID: 84941032259     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1384     Document Type: Article

References (46)

1. Aguilera,A. and Gomez-Gonzalez,B. (2008) Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet., 9, 204-217.
2. Ciccia,A. and Elledge,S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
3. Jackson,S.P. and Bartek,J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
4. Jackson,S.P. and Durocher,D. (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell, 49, 795-807.
5. Huertas,P. (2010) DNA resection in eukaryotes: deciding how to fix the break. Nat. Struct. Mol. Biol., 17, 11-16.
6. Lieber,M.R. (2008) The mechanism of human nonhomologous DNA end joining. J. Biol. Chem., 283, 1-5.
7. McVey,M. and Lee,S.E. (2008) MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet., 24, 529-538.
8. Heyer,W.D., Ehmsen,K.T. and Liu,J. (2010) Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet., 44, 113-139.
9. Huertas,P., Cortes-Ledesma,F., Sartori,A.A., Aguilera,A. and Jackson,S.P. (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature, 455, 689-692.
10. Huertas,P. and Jackson,S.P. (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem., 284, 9558-9565.
11. Rabut,G. and Peter,M. (2008) Function and regulation of protein neddylation. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep., 9, 969-976.
12. Huang,D.T., Ayrault,O., Hunt,H.W., Taherbhoy,A.M., Duda,D.M., Scott,D.C., Borg,L.A., Neale,G., Murray,P.J., Roussel,M.F. et al. (2009) E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification. Mol. Cell, 33, 483-495.
13. Ma,T., Chen,Y., Zhang,F., Yang,C.Y., Wang,S. and Yu,X. (2013) RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol. Cell, 49, 897-907.
14. Hannss,R. and Dubiel,W. (2011) COP9 signalosome function in the DDR. FEBS Lett., 585, 2845-2852.
15. Mendoza,H.M., Shen,L.N., Botting,C., Lewis,A., Chen,J., Ink,B. and Hay,R.T. (2003) NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem., 278, 25637-25643.
16. Duda,D.M., Scott,D.C., Calabrese,M.F., Zimmerman,E.S., Zheng,N. and Schulman,B.A. (2011) Structural regulation of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol., 21, 257-264.
17. Li,T., Guan,J., Huang,Z., Hu,X. and Zheng,X. (2014) RNF168-mediated H2A neddylation antagonizes its ubiquitination and regulates DNA damage repair. J. Cell Sci, 127, 2238-2248.
18. Xirodimas,D.P., Saville,M.K., Bourdon,J.C., Hay,R.T. and Lane,D.P. (2004) Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell, 118, 83-97.
19. Yang,D., Tan,M., Wang,G. and Sun,Y. (2012) The p21-dependent radiosensitization of human breast cancer cells by MLN4924, an investigational inhibitor of NEDD8 activating enzyme. PloS one, 7, e34079.
20. Cukras,S., Morffy,N., Ohn,T. and Kee,Y. (2014) Inactivating UBE2M impacts the DNA damage response and genome integrity involving multiple Cullin ligases. PloS one, 9, e101844.
21. Matsuoka,S., Ballif,B.A., Smogorzewska,A., McDonald,E.R. III, 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.
22. Gomez-Cabello,D., Jimeno,S., Fernandez-Avila,M.J. and Huertas,P. (2013) New tools to study DNA double-strand break repair pathway choice. PloS one, 8, e77206.
23. Pierce,A.J., Hu,P., Han,M., Ellis,N. and Jasin,M. (2001) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev., 15, 3237-3242.
24. 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.
25. Certo,M.T., Ryu,B.Y., Annis,J.E., Garibov,M., Jarjour,J., Rawlings,D.J. and Scharenberg,A.M. (2011) Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods, 8, 671-676.
26. Cruz-Garcia,A., Lopez-Saavedra,A. and Huertas,P. (2014) BRCA1 accelerates CtIP-mediated DNA-end resection. Cell Rep, 9, 451-459.
27. Yu,X. and Chen,J. (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol., 24, 9478-9486.
28. 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.
29. 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.
30. Poulsen,S.L., Hansen,R.K., Wagner,S.A., van Cuijk,L., van Belle,G.J., Streicher,W., Wikstrom,M., Choudhary,C., Houtsmuller,A.B., Marteijn,J.A. et al. (2013) RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol., 201, 797-807.
31. Miller,K.M., Tjeertes,J.V., Coates,J., Legube,G., Polo,S.E., Britton,S. and Jackson,S.P. (2010) Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol., 17, 1144-1151.
32. Murga,M., Jaco,I., Fan,Y., Soria,R., Martinez-Pastor,B., Cuadrado,M., Yang,S.M., Blasco,M.A., Skoultchi,A.I. and Fernandez-Capetillo,O. (2007) Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol., 178, 1101-1108.
33. Lord,C.J. and Ashworth,A. (2008) Targeted therapy for cancer using PARP inhibitors. Curr. Opin. Pharmacol., 8, 363-369.
34. Beck,C., Boehler,C., Barbat,J.G., Bonnet,M.E., Illuzzi,G., Ronde,P., Gauthier,L.R., Magroun,N., Rajendran,A., Lopez,B.S. et al. (2014) PARP3 affects the relative contribution of homologous recombination and nonhomologous end-joining pathways. Nucleic Acids Res, 42, 5616-5632.
35. Jazayeri,A., Balestrini,A., Garner,E., Haber,J.E. and Costanzo,V. (2008) Mre11-Rad50-Nbs1-dependent processing of DNA breaks generates oligonucleotides that stimulate ATMactivity. EMBO J., 27, 1953-1962.
36. Dupre,A., Boyer-Chatenet,L., Sattler,R.M., Modi,A.P., Lee,J.H., Nicolette,M.L., Kopelovich,L., Jasin,M., Baer,R., Paull,T.T. et al. (2008) A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat. Chem. Biol., 4, 119-125.
37. Cannavo,E. and Cejka,P. (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature, 514, 122-125.
38. Soucy,T.A., Smith,P.G., Milhollen,M.A., Berger,A.J., Gavin,J.M., Adhikari,S., Brownell,J.E., Burke,K.E., Cardin,D.P., Critchley,S. et al. (2009) An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature, 458, 732-736.
39. 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.
40. Shaheen,R., Faqeih,E., Ansari,S., Abdel-Salam,G., Al-Hassnan,Z.N., Al-Shidi,T., Alomar,R., Sogaty,S. and Alkuraya,F.S. (2014) Genomic analysis of primordial dwarfism reveals novel disease genes. Genome Res., 24, 291-299.
41. Qvist,P., Huertas,P., Jimeno,S., Nyegaard,M., Hassan,M.J., Jackson,S.P. and Borglum,A.D. (2011) CtIP mutations cause Seckel and Jawad syndromes. PLoS Genet., 7, e1002310.
42. Prado,F. and Aguilera,A. (2003) Control of cross-over by single-strand DNA resection. Trends Genet., 19, 428-431.
43. Blank,J.L., Liu,X.J., Cosmopoulos,K., Bouck,D.C., Garcia,K., Bernard,H., Tayber,O., Hather,G., Liu,R., Narayanan,U. et al. (2013) Novel DNA damage checkpoints mediating cell death induced by the NEDD8-activating enzyme inhibitor MLN4924. Cancer Res., 73, 225-234.
44. Liao,H., Liu,X.J., Blank,J.L., Bouck,D.C., Bernard,H., Garcia,K. and Lightcap,E.S. (2011) Quantitative proteomic analysis of cellular protein modulation upon inhibition of the NEDD8-activating enzyme by MLN4924. Mol. Cell. Proteomic., 10, M111 009183.
45. Narod,S.A. and Foulkes,W.D. (2004) BRCA1 and BRCA2: 1994 and beyond. Nat. Rev. Cancer, 4, 665-676.
46. Soria-Bretones,I., Saez,C., Ruiz-Borrego,M., Japon,M.A. and Huertas,P. (2013) Prognostic value of CtIP/RBBP8 expression in breast cancer. Cancer Med., 2, 774-783.