The RNF138 E3 ligase displaces Ku to promote DNA end resection and regulate DNA repair pathway choice

Nature Cell Biology

Volumn 17, Issue 11, 2015, Pages 1446-1457

  Ismail, Ismail Hassan ^a,b   Gagné, Jean Philippe ^c,d   Genois, Marie Michelle ^c,d   Strickfaden, Hilmar ^a   Mcdonald, Darin ^a   Xu, Zhizhong ^a   Poirier, Guy G ^c,d   Masson, Jean Yves ^c,d   Hendzel, Michael J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b CAIRO UNIVERSITY   (Egypt)

^c LAVAL UNIVERSITY   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; KU ANTIGEN; KU80 PROTEIN; MRE11 PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 RNF138; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, HUMAN; DNA; DNA HELICASE; PHOTOPROTEIN; PROTEIN BINDING; RNF138 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE; XRCC5 PROTEIN, HUMAN;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA END RESECTION; DNA FLANKING REGION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME REGULATION; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; RECOMBINATION REPAIR; RNA INTERFERENCE; S PHASE CELL CYCLE CHECKPOINT; U2OS CELL LINE; UBIQUITINATION; ZINC FINGER MOTIF; CONFOCAL MICROSCOPY; GENETICS; HEK293 CELL LINE; HELA CELL LINE; IMMUNOBLOTTING; MCF 7 CELL LINE; METABOLISM; MUTATION; TUMOR CELL LINE;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA HELICASES; DNA REPAIR; DNA, NEOPLASM; DNA, SINGLE-STRANDED; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOBLOTTING; LUMINESCENT PROTEINS; MCF-7 CELLS; MICROSCOPY, CONFOCAL; MUTATION; PROTEIN BINDING; RECOMBINATIONAL DNA REPAIR; RNA INTERFERENCE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84945973395     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3259     Document Type: Article

References (48)

1. Hartlerode A. J., & Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem. J. 423, 157-168 (2009
2. Pardo B., Gomez-Gonzalez B., & Aguilera A. DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell. Mol. Life Sci. 66, 1039-1056 (2009
3. Lieber M. R. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 283, 1-5 (2008
4. San Filippo J., Sung P., & Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257 (2008
5. Chapman J. R., Taylor M. R., & Boulton S. J. Playing the end game: DNA doublestrand break repair pathway choice. Mol. Cell 47, 497-510 (2012
6. Rodrigue A., et al. Interplay between human DNA repair proteins at a unique doublestrand break in vivo. EMBO J. 25, 222-231 (2006
7. Wu D., Topper L. M., & Wilson T. E. Recruitment and dissociation of nonhomologous end joining proteins at a DNA double-strand break in Saccharomyces cerevisiae. Genetics 178, 1237-1249 (2008
8. Shim E. Y., et al. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J. 29, 3370-3380 (2010
9. Symington L. S., & Gautier J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271 (2011
10. 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
11. Aylon Y., Liefshitz B., & Kupiec M. The CDK regulates repair of doublestrand breaks by homologous recombination during the cell cycle. EMBO J. 23, 4868-4875 (2004
12. Branzei D., & Foiani M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9, 297-308 (2008
13. Delacote F., Han M., Stamato T. D., Jasin M., & Lopez B. S. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by doublestrand breaks in mammalian cells. Nucl. Acids Res. 30, 3454-3463 (2002
14. Li W., et al. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelles dynamics and signaling. PLoS ONE 3, e1487 (2008
15. Karanam K., Kafri R., Loewer A., & Lahav G. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in mid S phase. Mol. Cell 47, 320-329 (2012
16. Essers J., et al. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21, 2030-2037 (2002
17. Katyal S., et al. Aberrant topoisomerase-1 DNA lesions are pathogenic in neurodegenerative genome instability syndromes. Nat. Neurosci. 17, 813-821 (2014
18. 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
19. Matsuoka S., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007
20. Shanbhag N. M., Rafalska-Metcalf I. U., Balane-Bolivar C., Janicki S. M., & Greenberg R. A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981 (2010
21. Loughlin F. E., & Mackay J. P. Zinc fingers are known as domains for binding DNA and RNA. Do they also mediate protein-protein interactions?. IUBMB Life 58, 731-733 (2006
22. Ismail I. H., et al. CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucl. Acids Res. 40, 5497-5510 (2012
23. 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
24. Ardley H. C., & Robinson P. A. E3 ubiquitin ligases. Essays Biochem. 41, 15-30 (2005
25. Feng L., & Chen J. The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat. Struct. Mol. Biol. 19, 201-206 (2012
26. Postow L., et al. Ku80 removal from DNA through double strand break-induced ubiquitylation. J. Cell Biol. 182, 467-479 (2008
27. Cheng Q., et al. Ku counteracts mobilization of PARP1 and MRN in chromatin damaged with DNA double-strand breaks. Nucl. Acids Res. 39, 9605-9619 (2011
28. Britton S., Coates J., & Jackson S. P. A new method for high-resolution imaging of Ku foci to decipher mechanisms of DNA double-strand break repair. J. Cell Biol. 202, 579-595 (2013
29. Bernstein K. A., & Rothstein R. At loose ends: resecting a double-strand break. Cell 137, 807-810 (2009
30. Zhou Y. X., et al. A novel gene RNF138 expressed in human gliomas and its function in the glioma cell line U251. Anal. Cell. Pathol. 35, 167-178 (2012
31. Cimprich K. A., & Cortez D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627 (2008
32. Raderschall E., Golub E. I., & Haaf T. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl Acad. Sci. USA 96, 1921-1926 (1999
33. Pierce A. J., Hu P., Han M., Ellis N., & Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242 (2001
34. Shao Z., et al. Persistently bound Ku at DNA ends attenuates DNA end resection and homologous recombination. DNA Repair 11, 310-316 (2012
35. Frank-Vaillant M., & Marcand S. Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell 10, 1189-1199 (2002
36. Kim J. S., et al. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol. 170, 341-347 (2005
37. Schmidt C. K., et al. Systematic E2 screening reveals a UBE2D-RNF138-CtIP axis promoting DNA repair. Nat. Cell Biol. 17, 1458-1470 (2015
38. Xie A., Kwok A., & Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 16, 814-818 (2009
39. Pierce A. J., Johnson R. D., Thompson L. H., & Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13, 2633-2638 (1999
40. Mendez J., & Stillman B. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20, 8602-8612 (2000
41. Maity R., et al. GST-His purification: a two-step affinity purification protocol yielding full-length purified proteins. J. Vis. Exp. e50320 (2013
42. Ismail I. H., et al. CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucl. Acids Res. 40, 5497-5510 (2012
43. Menard L., & Poirier G. G. Rapid assay of poly(ADP-ribose) glycohydrolase. Biochem. Cell Biol. 65, 668-673 (1987
44. Shevchenko A., Wilm M., Vorm O., & Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996
45. Havlis J., Thomas H., Sebela M., & Shevchenko A. Fast-response proteomics by accelerated in-gel digestion of proteins. Anal. Chem. 75, 1300-1306 (2003
46. Shilov I. V., et al. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell Proteomics 6, 1638-1655 (2007
47. Keller A., Nesvizhskii A. I., Kolker E., & Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (2002
48. Nesvizhskii A. I., Keller A., Kolker E., & Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (2003