Systematic E2 screening reveals a UBE2D-RNF138-CtIP axis promoting DNA repair

Nature Cell Biology

Volumn 17, Issue 11, 2015, Pages 1458-1470

  Schmidt, Christine K ^a   Galanty, Yaron ^a   Sczaniecka Clift, Matylda ^a   Coates, Julia ^a   Jhujh, Satpal ^a   Demir, Mukerrem ^a   Cornwell, Matthew ^a   Beli, Petra ^b   Jackson, Stephen P ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; BRCA1 PROTEIN; CAMPTOTHECIN; CELL PROTEIN; CHECKPOINT KINASE 1; CTIP PROTEIN; KAP1 PROTEIN; RING FINGER PROTEIN; RING FINGER PROTEIN 138; RPA2 PROTEIN; UBE2D PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; NUCLEAR PROTEIN; RBBP8 PROTEIN, HUMAN; RNF138 PROTEIN, HUMAN; UBE2D1 PROTEIN, HUMAN; UBE2D2 PROTEIN, HUMAN; UBE2D3 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME INHIBITION; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECOMBINATION REPAIR; SEQUENCE HOMOLOGY; UBIQUITINATION; CELL CYCLE; CELL SURVIVAL; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; METABOLISM; RADIATION RESPONSE; RNA INTERFERENCE; TUMOR CELL LINE;

CARRIER PROTEINS; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; MICROSCOPY, CONFOCAL; NUCLEAR PROTEINS; RECOMBINATIONAL DNA REPAIR; RNA INTERFERENCE; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84945937533     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3260     Document Type: Article

References (70)

1. Jackson S. P., & Bartek J. The DNA-damage response in human biology and disease. Nature 461, 1071-1078 (2009
2. Ciccia A., & Elledge S. J. The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204 (2010
3. Deriano L., & Roth D. B. Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu. Rev. Genet. 47, 433-455 (2013
4. Sartori A. A., et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007
5. Greenberg R. A., et al. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20, 34-46 (2006
6. Shiloh Y., & Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 14, 197-210 (2013
7. Polo S. E., & Jackson S. P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433 (2011
8. Jackson S. P., & Durocher D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795-807 (2013
9. Kulathu Y., & Komander D. Atypical ubiquitylation-the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 13, 508-523 (2012
10. Husnjak K., & Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322 (2012
11. Wenzel D. M., Stoll K. E., & Klevit R. E. E2s: structurally economical and functionally replete. Biochem. J. 433, 31-42 (2011
12. Ye Y., & Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764 (2009
13. Povlsen L. K., et al. Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nat. Cell Biol. 14, 1089-1098 (2012
14. Certo M. T., et al. Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods 8, 671-676 (2011
15. Davies O. R., et al. CtIP tetramer assembly is required for DNA-end resection and repair. Nat. Struct. Mol. Biol. 22, 150-157 (2015
16. Jazayeri A., et al. ATM-and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45 (2006
17. Murakawa Y., et al. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 67, 8536-8543 (2007
18. Zhou Y., Caron P., Legube G., & Paull T. T. Quantitation of DNA doublestrand break resection intermediates in human cells. Nucleic Acids Res. 42, e19 (2014
19. Polato F., et al. CtIP-mediated resection is essential for viability and can operate independently of BRCA1. J. Exp. Med. 211, 1027-1036 (2014
20. Kakarougkas A., et al. Co-operation of BRCA1 and POH1 relieves the barriers posed by 53BP1 and RAP80 to resection. Nucleic Acids Res. 41, 10298-10311 (2013
21. Long D. T., Joukov V., Budzowska M., & Walter J. C. BRCA1 promotes unloading of the CMG Helicase from a stalled DNA replication Fork. Mol. Cell 56, 1-12 (2014
22. Cruz-García A., López-Saavedra A., & Huertas P. BRCA1 accelerates CtIP-mediated DNA-End resection. Cell Rep. 9, 451-459 (2014
23. Machida Y. J., et al. UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol. Cell 23, 589-596 (2006
24. Zhang Y., et al. UBE2W interacts with FANCL and regulates the monoubiquitination of Fanconi anemia protein FANCD2. Mol. Cell 31, 113-122 (2011
25. Maréchal A., et al. PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol. Cell 53, 235-246 (2014
26. Adamson B., Smogorzewska A., Sigoillot F. D., King R. W., & Elledge S. J. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol. 14, 318-328 (2012
27. Ikura T., et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27, 7028-7040 (2007
28. Liu C., et al. RNF168 forms a functional complex with RAD6 during the DNA damage response. J. Cell Sci. 126, 2042-2051 (2013
29. Jacquemont C., & Taniguchi T. Proteasome function is required for DNA damage response and Fanconi anemia pathway activation. Cancer Res. 67, 7395-7405 (2007
30. Matsuoka S., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007
31. Gudjonsson T., et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697-709 (2012
32. Parsons J. L., et al. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 29, 477-487 (2008
33. Inagaki A., et al. Human RAD18 interacts with ubiquitylated chromatin components and facilitates RAD9 recruitment to DNA double strand breaks. PLoS ONE 6, e23155 (2011
34. Watanabe K., et al. RAD18 promotes DNA double-strand break repair during G1 phase through chromatin retention of 53BP1. Nucleic Acids Res. 37, 2176-2193 (2009
35. Giannini A. L., Gao Y., & Bijlmakers M.-J. T-cell regulator RNF125/TRAC-1 belongs to a novel family of ubiquitin ligases with zinc fingers and a ubiquitin-binding domain. Biochem. J. 410, 101-111 (2008
36. Yamada M., et al. NARF, an nemo-like kinase (NLK)-associated ring finger protein regulates the ubiquitylation and degradation of T cell factor/lymphoid enhancer factor (TCF/LEF). J. Biol. Chem. 281, 20749-20760 (2006
37. Polanowska J., Martin J. S., Garcia-Muse T., Petalcorin M. I. R., & Boulton S. J. A conserved pathway to activate BRCA1-dependent ubiquitylation at DNA damage sites. EMBO J. 25, 2178-2188 (2006
38. You Z., et al. CtIP links DNA double-strand break sensing to resection. Mol. Cell 36, 954-969 (2009
39. Morris J. R., & Solomon E. BRCA1: BARD1 induces the formation of conjugated ubiquitin structures, dependent on K6 of ubiquitin, in cells during DNA replication and repair. Hum. Mol. Genet. 13, 807-817 (2004
40. Kaidi A., Weinert B. T., Choudhary C., & Jackson S. P. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329, 1348-1353 (2010
41. Andres S. N., et al. Tetrameric Ctp1 coordinates DNA binding and DNA bridging in DNA double-strand-break repair. Nat. Struct. Mol. Biol. 22, 158-166 (2015
42. Murina O., et al. FANCD2 and CtIP cooperate to repair DNA interstrand crosslinks. Cell Rep. 7, 1030-1038 (2014
43. Ismail I. H., et al. RNF138 is an E3 ubiquitin ligase that displaces Ku to promote DNA end resection and regulate DNA repair pathway choice. Nat. Cell Biol. 17, 1446-1447 (2015
44. Galanty Y., Belotserkovskaya R., Coates J., & Jackson S. P. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195 (2012
45. Smeenk G., et al. Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J. Cell Sci. 126, 889-903 (2013
46. Markson G., et al. Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res. 19, 1905-1911 (2009
47. Gao J., et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6, pl1 (2013
48. Paulsen R. D., et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell 35, 228-239 (2009
49. Curtin N. J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer 12, 801-817 (2012
50. Mattern M. R., Wu J., & Nicholson B. Ubiquitin-based anticancer therapy: carpet bombing with proteasome inhibitors vs surgical strikes with E1, E2, E3, or DUB inhibitors. Biochim. Biophys. Acta 1823, 2014-2021 (2012
51. Krzywinski M., et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009
52. You Z., & Bailis J. M. DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol. 20, 402-409 (2010
53. Limoli C. L., & Ward J. F. A new method for introducing double-strand breaks into cellular DNA. Radiat. Res. 134, 160-169 (1993
54. Lukas C., Falck J., Bartkova J., Bartek J., & Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5, 255-260 (2003
55. Hodson C., Purkiss A., Miles J. A., & Walden H. Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3-E2 selection. Structure 22, 337-344 (2014
56. Michalski A., et al. Mass spectrometry-based proteomics using Q Exactive, a highperformance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell. Proteomics 10, M111.011015 (2011
57. Cox J., & Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008
58. Cox J., et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805 (2011
59. Shibata E., Abbas T., Huang X., Wohlschlegel J. a, & Dutta A. Selective ubiquitylation of p21 and Cdt1 by UBCH8 and UBE2G ubiquitin-conjugating enzymes via the CRL4Cdt2 ubiquitin ligase complex. Mol. Cell. Biol. 31, 3136-45 (2011
60. Zhong Q., Gao W., Du F., & Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121, 1085-95 (2005
61. Doil C., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-46 (2009
62. Galanty Y., et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-9 (2009
63. Biton S., et al. Nuclear ataxia-telangiectasia mutated (ATM) mediates the cellular response to DNA double strand breaks in human neuron-like cells. J. Biol. Chem. 281, 17482-91 (2006
64. Bruun D., et al. siRNA depletion of BRCA1, but not BRCA2, causes increased genome instability in Fanconi anemia cells. DNA Repair (Amst). 2, 1007-1013 (2003
65. 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, 858-71 (2013
66. Biard D. S. F. Untangling the relationships between DNA repair pathways by silencing more than 20 DNA repair genes in human stable clones. Nucleic Acids Res. 35, 3535-50 (2007
67. Liang L., et al. Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks. Nucleic Acids Res. 36, 3297-310 (2008
68. Ito M., et al. Rad51 siRNA delivered by HVJ envelope vector enhances the anti-cancer effect of cisplatin. J. Gene Med. 7, 1044-1052 (2005
69. Lubas M., et al. Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell 43, 624-37 (2011
70. Michelle C., Vourch, P., Mignon L., & Andres C. R. What was the set of ubiquitin and ubiquitin-like conjugating enzymes in the eukaryote common ancestor?. J. Mol. Evol. 68, 616-28 (2009