NBA1, a new player in the Brcal A complex, is required for DNA damage resistance and checkpoint control

Genes and Development

Volumn 23, Issue 6, 2009, Pages 729-739

  Wang, Bin ^a,b   Hurov, Kristen ^a   Hofmann, Kay ^c   Elledge, Stephen J ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c MILTENYI BIOTEC GMBH   (Germany)

Author keywords

Abraxas; BRCA1 A complex; MPN domain; Proteasome; VWA domain

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; GENE PRODUCT; POLYUBIQUITIN; PROTEIN BRCC36; PROTEIN NBA1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; DNA DAMAGE; GENE IDENTIFICATION; GENETIC SCREENING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IONIZING RADIATION; NBA1 GENE; ONCOGENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOMICS;

AMINO ACID SEQUENCE; BRCA1 PROTEIN; CARRIER PROTEINS; CELL CYCLE; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; HUMANS; LASERS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; POLYUBIQUITIN; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITINATION;

EID: 63049138322     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1770309     Document Type: Article

References (42)

1. Ambroggio, X.I., Rees, D.C., and Deshaies, R.J. 2004. JAMM: A metalloprotease-like zinc site in the proteasome and signal-osome. PLoS Biol. 2: E2. doi:10.1371/journal.pbio.0020002.
2. Baer, R. and Ludwig, T. 2002. The BRCA 1/BARD 1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12: 86-91.
3. Chen, X., Arciero, C.A., Wang, C, Broccoli, D., and Godwin, A.K. 2006. BRCC36 is essential for ionizing radiation-induced BRCA1 phosphorylation and nuclear foci formation. Cancer Res. 66: 5039-5046.
4. Cope, G.A. and Deshaies, R.J. 2003. COP9 signalosome: A multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell 114: 663-671.
5. Doherty, A.J. and Jackson, S.R 2001. DNA repair: How Ku makes ends meet. Curr. Biol. 11: R920-R924. doi:10.1016/ S0960-9822(01 (00555-3.
6. Dong, Y., Hakimi, M.A., Chen, X., Kumaraswamy, E., Cooch, N.S., Godwin, A.K., and Shiekhattar, R. 2003. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell 12: 1087-1099.
7. Elsasser, S. and Finley, D. 2005. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7: 742-749.
8. Fu, H., Reis, N., Lee, Y., Glickman, M.H., and Vierstra, R.D. 2001. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 20: 7096-7107.
9. Glickman, M.H., Rubin, D.M., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Baumeister, W., Fried, V.A., and Finley, D. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-eonjugate degradation and related to the COP9-signalosome and eIF3. Cell 94: 615-623.
10. Greenberg, R.A., Sobhian, B., Pathania, S., Cantor, S.B., Naka-tani, Y., and Livingston, D.M. 2006. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes & Dev. 20: 34-46.
11. Hamazaki, J., Sasaki, K., Kawahara, H., Hisanaga, S., Tanaka, K., and Murata, S. 2007. Rpnl0-mediated degradation of ubiquitinated proteins is essential for mouse development. Mol. Cell. Biol. 27: 6629-6638.
12. Harper, J.W. and Elledge, S.J. 2007. The DNA damage response: Ten years after. Mol Cell 28: 739-745.
13. 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.
14. Hofmann, K. and Bucher, P. 1998. The PCI domain: A common theme in three multiprotein complexes. Trends Biochem. Sci. 23: 204-205.
15. Hofmann, K. and Falquet, L. 2001. A ubiquitin-interaeting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26: 347- 350.
16. 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.
17. Hurley, J.H., Lee, S., and Prag, G. 2006. Ubiquitin-binding domains. Biochem. J. 399: 361-372.
18. Kim, H., Chen, J., and Yu, X. 2007. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316: 1202-1205.
19. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M., et al. 2007. Orchestration of the DNA- damage response by the RNF8 ubiquitin ligase. Science 318: 1637-1640.
20. Lam, Y.A., Lawson, T.G., Velayutham, M., Zweier, J.L., and Pickart, CM. 2002. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416: 763- 767.
21. Mailand, N., Bekker-fensen, 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.
22. +, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpnll function. BMC Biochem. 3: 28. doi: 10.1186/1471-2091-3-28.
23. Narod, S.A. and Foulkes, W.D. 2004. BRCA1 and BRCA2: 1994 and beyond. Nat. Rev. Cancer 4: 665-676.
24. Paddison, P.J., Silva, J.M., Conklin, D.S., Schlabach, M., Li, M., Aruleba, S., Balija, V., O'Shaughnessy, A., Gnoj, L., Scobie, K., et al. 2004, A resource for large-scale RNA-interference- based screens in mammals. Nature 428: 427-431.
25. Rual, J.F., Venkatesan, K., Hao, T, Hirozane-Kishikawa, T., Dricot, A., Li, N., Berriz, G.F., Gibbons, F.D., Dreze, M., Ayivi-Guedehoussou, N., et al, 2005. Towards a proteome- scale map of the human protein-protein interaction network. Nature 437: 1173-1178.
26. Ruffner, H., Joazeiro, C.A., Hemmati, D., Hunter, T., and Verma, I.M. 2001. Cancer-predisposing mutations within the RING domain of BRCA1: Loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc. Natl. Acad. Sci. 98: 5134-5139.
27. Scheel, H. and Hofmann, K. 2005. Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinformatics 6:71. doi: 10.1186/1471-2105- 6-71.
28. Schlabach, M.R., Luo, J., Solimini, N.L., Hu, G., Xu, Q., Li, M.Z., Zhao, Z., Smogorzewska, A., Sowa, M.E., Ang, X.L., et al. 2008. Cancer proliferation gene discovery through functional genomics. Science 319: 620-624.
29. Silva, J.M., Li, M.Z., Chang, K., Ge, W., Golding, M.C., Rickles, R.J., Siolas, D., Hu, G., Paddison, P.J., Schlabach, M.R., et al. 2005. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 37: 1281-1288.
30. Silva, J.M., Marran, K., Parker, J.S., Silva, J., Golding, M., Schlabach, M.R., Elledge, S.J., Harmon, G.J., and Chang, K. 2008. Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319: 617-620.
31. Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, 3rd, E.R. Hurov, K.E., Luo, J., Ballif, B.A., Gygi, S.P., Hofmann, K., D'Andrea, A.D., et al. 2007. Identification of the FANCI protein, a monoubiqutinated FANCD2 paralog required for DNA repair. Cell 129: 289-301.
32. Sobhian, B., Shao, G., Lilli, D.R., Culhane, A.C., Moreau, L.A., Xia, B., Livingston, D.M., and Greenberg, RA. 2007. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316: 1198-1202.
33. Venkitaraman, A.R. 2002. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108: 171-182.
34. Verma, R., Aravind, L., Oania, R., McDonald, W.H., Yates, III, J.R. Koonin, E.V., and Deshaies, R.J. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298: 611-615.
35. Verma, R., Oania, R., Graumann, J., and Deshaies, R.J. 2004. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system, Cell 118:99-110.
36. Wang, B. and Elledge, S.J. 2007. Ubcl3/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brcal/Brcc36 complex in response to DNA damage. Pioc. Natl. Acad. Sci. 104: 20759-20763.
37. 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.
38. Wu, L.C., Wang, Z.W., Tsan, J.T., Spillman, M.A., Phung, A., Xu, X.L., Yang, M.C., Hwang, L.Y., Bowcock, A.M., and Baer, R. 1996. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat. Genet. 14:430-440.
39. Yan, J., Kim, Y.S., Yang, X.P., Albers, M., Koegl, M., and Jetten, A.M. 2007. Ubiquitin-interaction motifs of RAP80 are critical in its regulation of estrogen receptor α. Nucleic Acids Res. 35: 1673-1686.
40. Yao, T. and Cohen, R.E. 2002. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419: 403-407.
41. 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.
42. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.