The RING finger protein RNF8 ubiquitinates Nbs1 to promote DNA double-strand break repair by homologous recombination

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43984-43994

  Lu, Chi Sheng ^a   Truong, Lan N ^a   Aslanian, Aaron ^a,b   Shi, Linda Z ^c   Li, Yongjiang ^a   Hwang, Patty Yi Hwa ^a   Koh, Kwi Hye ^a   Hunter, Tony ^b   Yates III, John R ^a   Berns, Michael W ^c   Wu, Xiaohua ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

DNA DAMAGE RESPONSE; DNA DOUBLE STRAND BREAKS; HOMOLOGOUS RECOMBINATION; KEY REGULATORS; LIVE-CELL IMAGING; OPTIMAL BINDING; UBIQUITIN LIGASES; UBIQUITINATION;

DNA;

DNA; NIBRIN; PROTEIN RNF8; RING FINGER PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENETIC REGULATION; IMAGING; INVESTIGATIVE PROCEDURES; LASER MICROIRRADIATION; LIVE CELL IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RECOMBINATION REPAIR; UBIQUITINATION;

EID: 84871559319     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421545     Document Type: Article

References (62)

1. Symington, L. S., and Gautier, J. (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271
2. Pâques, F., and Haber, J. E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404 (Pubitemid 29264976)
3. Moynahan, M. E., and Jasin, M. (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11, 196-207
4. Lieber, M. R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211
5. 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
6. Nussenzweig, A., and Nussenzweig, M. C. (2007) A backup DNA repair pathway moves to the forefront. Cell 131, 223-225 (Pubitemid 47576147)
7. Xie, A., Kwok, A., and Scully, R. (2009) Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 16, 814-818
8. Rass, E., Grabarz, A., Plo, I., Gautier, J., Bertrand, P., and Lopez, B. S. (2009) Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 16, 819-824
9. Dinkelmann, M., Spehalski, E., Stoneham, T., Buis, J., Wu, Y., Sekiguchi, J. M., and Ferguson, D. O. (2009) Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol. 16, 808-813
10. 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
11. Wang, H., Shao, Z., Shi, L. Z., Hwang, P. Y., Truong, L. N., Berns, M. W., Chen, D. J., and Wu, X. (2012) CtIP protein dimerization is critical for its recruitment to chromosomal DNA double-stranded breaks. J. Biol. Chem. 287, 21471-21480
12. D'Amours, D., and Jackson, S. P. (2002) The Mre11 complex. At the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3, 317-327 (Pubitemid 34619266)
13. Lee, J. H., and Paull, T. T. (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26, 7741-7748
14. Uziel, T., Lerenthal, Y., Moyal, L., Andegeko, Y., Mittelman, L., and Shiloh, Y. (2003) Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22, 5612-5621 (Pubitemid 37279970)
15. Polo, S. E., and Jackson, S. P. (2011) Dynamics of DNA damage response proteins at DNA breaks. A focus on protein modifications. Genes Dev. 25, 409-433
16. Stucki, M., Clapperton, J. A., Mohammad, D., Yaffe, M. B., Smerdon, S. J., and Jackson, S. P. (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (Pubitemid 41821780)
17. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., and Lukas, J. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900 (Pubitemid 350138084)
18. Chapman, J. R., and Jackson, S. P. (2008) Phospho-dependent interactions between NBS1 andMDC1mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 9, 795-801
19. Wu, L., Luo, K., Lou, Z., and Chen, J. (2008)MDC1regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 105, 11200-11205
20. Melander, F., Bekker-Jensen, S., Falck, J., Bartek, J., Mailand, N., and Lukas, J. (2008) Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 181, 213-226 (Pubitemid 351574548)
21. Spycher, C., Miller, E. S., Townsend, K., Pavic, L., Morrice, N. A., Janscak, P., Stewart, G. S., and Stucki, M. (2008) Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 181, 227-240 (Pubitemid 351574549)
22. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M. J., Pilch, D. R., Staudt, D. W., Lee, A., Bonner, R. F., Bonner, W. M., and Nussenzweig, A. (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5, 675-679 (Pubitemid 36818091)
23. Lukas, C., Melander, F., Stucki, M., Falck, J., Bekker-Jensen, S., Goldberg, M., Lerenthal, Y., Jackson, S. P., Bartek, J., and Lukas, J. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674-2683 (Pubitemid 38988238)
24. Al-Hakim, A., Escribano-Diaz, C., Landry, M. C., O'Donnell, L., Panier, S., Szilard, R. K., and Durocher, D. (2010) The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair 9, 1229-1240
25. Messick, T. E., and Greenberg, R. A. (2009) The ubiquitin landscape at DNA double-strand breaks. J. Cell Biol. 187, 319-326
26. Brzovic, P. S., Rajagopal, P., Hoyt, D. W., King, M. C., and Klevit, R. E. (2001) Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat. Struct. Biol. 8, 833-837 (Pubitemid 32923599)
27. Hashizume, R., Fukuda, M., Maeda, I., Nishikawa, H., Oyake, D., Yabuki, Y., Ogata, H., and Ohta, T. (2001) The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276, 14537-14540
28. Nishikawa, H., Ooka, S., Sato, K., Arima, K., Okamoto, J., Klevit, R. E., Fukuda, M., and Ohta, T. (2004) Mass spectrometric and mutational analyses reveal Lys-6-linked polyubiquitin chains catalyzed by BRCA1-BARD1 ubiquitin ligase. J. Biol. Chem. 279, 3916-3924 (Pubitemid 38198974)
29. Wu-Baer, F., Lagrazon, K., Yuan, W., and Baer, R. (2003) The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. J. Biol. Chem. 278, 34743-34746 (Pubitemid 37102231)
30. Plans, V., Scheper, J., Soler, M., Loukili, N., Okano, Y., and Thomson, T. M. (2006) The RING finger protein RNF8 recruits UBC13 for lysine 63-based self polyubiquitylation. J. Cell Biochem. 97, 572-582 (Pubitemid 43265316)
31. Zhang, S., Chea, J., Meng, X., Zhou, Y., Lee, E. Y., and Lee, M. Y. (2008) PCNA is ubiquitinated by RNF8. Cell Cycle 7, 3399-3404
32. Feng, L., and Chen, J. (2012) The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat. Struct. Mol. Biol. 19, 201-206
33. 63-based poly-ubiquitylation. Nucleic Acids Res. 40, 196-205
34. Bekker-Jensen, S., Rendtlew Danielsen, J., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bartek, J., Lukas, J., and Mailand, N. (2010) HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 12, 80-86
35. Ito, K., Adachi, S., Iwakami, R., Yasuda, H., Muto, Y., Seki, N., and Okano, Y. (2001) N-terminally extended human ubiquitin-conjugating enzymes (E2s) mediate the ubiquitination of RING-finger proteins, ARA54 and RNF8. Eur. J. Biochem. 268, 2725-2732 (Pubitemid 32853012)
36. Huen, M. S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M. B., and Chen, J. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901-914 (Pubitemid 350138083)
37. Kolas, N. K., Chapman, J. R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F. D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T. M., Pelletier, L., Jackson, S. P., and Durocher, D. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637-1640 (Pubitemid 350233664)
38. Wang, B., and Elledge, S. J. (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 104, 20759-20763
39. Kim, H., Chen, J., and Yu, X. (2007) Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205 (Pubitemid 46877484)
40. 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 (Pubitemid 46877483)
41. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P., and Elledge, S. J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194-1198 (Pubitemid 46877482)
42. Yan, J., Kim, Y. S., Yang, X. P., Li, L. P., Liao, G., Xia, F., and Jetten, A. M. (2007) The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res. 67, 6647-6656 (Pubitemid 47105510)
43. 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., Oldreive, C., Wildenhain, J., Tagliaferro, A., Pelletier, L., Taubenheim, N., Durandy, A., Byrd, P. J., Stankovic, T., Taylor, A. M., and Durocher, D. (2009) The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434
44. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D. H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., Lukas, J., and Lukas, C. (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446
45. Olson, E., Nievera, C. J., Lee, A. Y., Chen, L., and Wu, X. (2007) The Mre11-Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangiectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment. J. Biol. Chem. 282, 22939-22952 (Pubitemid 47267303)
46. Ai, H. W., Shaner, N. C., Cheng, Z., Tsien, R. Y., and Campbell, R. E. (2007) Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry 46, 5904-5910 (Pubitemid 46799153)
47. Olson, E., Nievera, C. J., Liu, E., Lee, A. Y., Chen, L., and Wu, X. (2007) The Mre11 complex mediates the S-phase checkpoint through an interaction with replication protein A. Mol. Cell Biol. 27, 6053-6067 (Pubitemid 47326694)
48. Chen, L., Nievera, C. J., Lee, A. Y., and Wu, X. (2008) Cell cycle-dependent complex formation of BRCA1·CtIP·MRN is important for DNA double-strand break repair. J. Biol. Chem. 283, 7713-7720
49. Wu, X., Avni, D., Chiba, T., Yan, F., Zhao, Q., Lin, Y., Heng, H., and Livingston, D. (2004) SV40 T antigen interacts with Nbs1 to disrupt DNA replication control. Genes Dev. 18, 1305-1316 (Pubitemid 38720598)
50. Wu, X., Ranganathan, V., Weisman, D. S., Heine, W. F., Ciccone, D. N., O'Neill, T. B., Crick, K. E., Pierce, K. A., Lane, W. S., Rathbun, G., Livingston, D. M., and Weaver, D. T. (2000) ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405, 477-482 (Pubitemid 30367426)
51. Paull, T. T., and Gellert, M. (1998) The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979 (Pubitemid 128379258)
52. Botvinick, E. L., and Berns, M. W. (2005) Internet-based robotic laser scissors and tweezers microscopy. Microsc. Res. Tech. 68, 65-74 (Pubitemid 41566388)
53. McDonald, W. H., Tabb, D. L., Sadygov, R. G., MacCoss, M. J., Venable, J., Graumann, J., Johnson, J. R., Cociorva, D., and Yates, J. R., 3rd (2004) MS1, MS2, and SQT. Three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun. Mass Spectrom. 18, 2162-2168 (Pubitemid 39222458)
54. Eng, J. K., Mccormack, A. L., and Yates, J. R., 3rd (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989
55. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., and Gygi, S. P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis. The yeast proteome. J. Proteome Res. 2, 43-50 (Pubitemid 36207189)
56. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd (2002) DTASelect and contrast. Tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
57. Wu, J., Zhang, X., Zhang, L., Wu, C. Y., Rezaeian, A. H., Chan, C. H., Li, J. M., Wang, J., Gao, Y., Han, F., Jeong, Y. S., Yuan, X., Khanna, K. K., Jin, J., Zeng, Y. X., and Lin, H. K. (2012) Skp2 E3 ligase integratesATMactivation and homologous recombination repair by ubiquitinating NBS1. Mol. Cell 46, 351-361
58. Buis, J., Wu, Y., Deng, Y., Leddon, J., Westfield, G., Eckersdorff, M., Sekiguchi, J. M., Chang, S., and Ferguson, D. O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135, 85-96
59. Panier, S., and Durocher, D. (2009) Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair 8, 436-443
60. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C., Lukas, J., and Jackson, S. P. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45 (Pubitemid 43064795)
61. Harper, J. W., and Schulman, B. A. (2006) Structural complexity in ubiquitin recognition. Cell 124, 1133-1136
62. Hicke, L., Schubert, H. L., and Hill, C. P. (2005) Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6, 610-621 (Pubitemid 41081265)