An interaction network of the mammalian COP9 signalosome identifies Dda1 as a core subunit of multiple Cul4-based E3 ligases

Journal of Cell Science

Volumn 122, Issue 7, 2009, Pages 1035-1044

  Olma, Michael Hans ^a   Roy, Marcia ^b,f   Le Bihan, Thierry ^c   Sumara, Izabela ^a   Maerki, Sarah ^a   Larsen, Brett ^b   Quadroni, Manfredo ^d   Peter, Matthias ^a   Tyers, Mike ^b   Pintard, Lionel ^b,e  

^a ETH ZURICH   (Switzerland)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Centre Intégratif de Génomique Plateforme de Protéomique   (Switzerland)

^e INSTITUT JACQUES MONOD   (France)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cullin RING E3 ligases; Dda1; Deneddylation; Neddylation; Ubiquitin dependent proteolysis

Indexed keywords

COP9 SIGNALOSOME; CULLIN; CULLIN 4; DOUBLE STRANDED DNA; GENE PRODUCT; PROTEIN DDA1; PROTEIN SUBUNIT; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CUL4A PROTEIN, HUMAN; CUL4B PROTEIN, HUMAN; DDA1 PROTEIN, HUMAN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; PEPTIDE HYDROLASE; PROTEOME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TANDEM MASS SPECTROMETRY; ANIMAL; CELL CYCLE; CELL LINE; CHROMATIN; MAMMAL; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT;

MAMMALIA;

ANIMALS; CELL CYCLE; CELL LINE; CHROMATIN; CULLIN PROTEINS; DNA-BINDING PROTEINS; HUMANS; MAMMALS; MULTIPROTEIN COMPLEXES; PEPTIDE HYDROLASES; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTEOME; UBIQUITIN-PROTEIN LIGASES;

EID: 66849097663     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.043539     Document Type: Article

References (40)

1. Angers, S., Li, T., Yi, X., MacCoss, M. J., Moon, R. T. and Zheng, N. (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593.
2. Bornstein, G., Ganoth, D. and Hershko, A. (2006). Regulation of neddylation and deneddylation of cullin1 in SCFSkp2 ubiquitin ligase by F-box protein and substrate. Proc. Natl. Acad. Sci. USA 103, 11515-11520.
3. Chew, E. H. and Hagen, T. (2007). Substrate-mediated regulation of cullin neddylation. J. Biol. Chem. 282, 17032-17040.
4. Duda, D. M., Borg, L. A., Scott, D. C., Hunt, H. W., Hammel, M. and Schulman, B. A. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006.
5. Fang, L., Wang, X., Yamoah, K., Chen, P. L., Pan, Z. Q. and Huang, L. (2008). Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J. Proteome Res. 7, 4914-4925.
6. Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A. F., Tanaka, K. and Nakatani, Y. (2003). The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357-367.
7. Higa, L. A. and Zhang, H. (2007). Stealing the spotlight: CUL4-DDB1 ubiquitin ligase docks WD40-repeat proteins to destroy. Cell Div. 2, 5.
8. Hong, E. J., Villen, J., Gerace, E. L., Gygi, S. P. and Moazed, D. (2005). A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol. 2, 106-111.
9. Hrecka, K., Gierszewska, M., Srivastava, S., Kozaczkiewicz, L., Swanson, S. K., Florens, L., Washburn, M. P. and Skowronski, J. (2007). Lentiviral Vpr usurps Cul4-DDB1[VprBP] E3 ubiquitin ligase to modulate cell cycle. Proc. Natl. Acad. Sci. USA 104, 11778-11783.
10. Huang, X., Hetfeld, B. K., Seifert, U., Kahne, T., Kloetzel, P. M., Naumann, M., Bech-Otschir, D. and Dubiel, W. (2005). Consequences of COP9 signalosome and 26S proteasome interaction. FEBS J. 272, 3909-3917.
11. Jin, J., Arias, E. E., Chen, J., Harper, J. W. and Walter, J. C. (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709-721.
12. Keller, A., Nesvizhskii, A. I., Kolker, E. and Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392.
13. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W. and Hedgecock, E. M. (1996). cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839.
14. Le Bihan, T., Duewel, H. S. and Figeys, D. (2003). On-line strong cation exchange micro-HPLC-ESI-MS/MS for protein identification and process optimization. J. Am. Soc. Mass Spectrom. 14, 719-727.
15. Licklider, L. J., Thoreen, C. C., Peng, J. and Gygi, S. P. (2002). Automation of nanoscale microcapillary liquid chromatography-tandem mass spectrometry with a vented column. Anal. Chem. 74, 3076-3083.
16. Liu, C., Poitelea, M., Watson, A., Yoshida, S. H., Shimoda, C., Holmberg, C., Nielsen, O. and Carr, A. M. (2005). Transactivation of Schizosaccharomyces pombe cdt2+ stimulates a Pcu4-Ddb1-CSN ubiquitin ligase. EMBO J. 24, 3940-3951.
17. Luke-Glaser, S., Roy, M., Larsen, B., Le Bihan, T., Metalnikov, P., Tyers, M., Peter, M. and Pintard, L. (2007). CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol. Cell. Biol. 27, 4526-4540.
18. Luke, B., Versini, G., Jaquenoud, M., Zaidi, I. W., Kurz, T., Pintard, L., Pasero, P. and Peter, M. (2006). The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16, 786-792.
19. Lyapina, S., Cope, G., Shevchenko, A., Serino, G., Tsuge, T., Zhou, C., Wolf, D. A., Wei, N. and Deshaies, R. J. (2001). Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292, 1382-1385.
20. Mahalingam, S., Ayyavoo, V., Patel, M., Kieber-Emmons, T., Kao, G. D., Muschel, R. J. and Weiner, D. B. (1998). HIV-1 Vpr interacts with a human 34-kDa mov34 homologue, a cellular factor linked to the G2/M phase transition of the mammalian cell cycle. Proc. Natl. Acad. Sci. USA 95, 3419-3424.
21. Mahrour, N., Redwine, W. B., Florens, L., Swanson, S. K., Martin-Brown, S., Bradford, W. D., Staehling-Hampton, K., Washburn, M. P., Conaway, R. C. and Conaway, J. W. (2008). Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J. Biol. Chem. 283, 8005-8013.
22. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., 3rd, 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.
23. McCall, C. M., Miliani de Marval, P. L., Chastain, P. D. n., Jackson, S. C., He, Y. J., Kotake, Y., Cook, J. G. and Xiong, Y. (2008). HIV-1 Vpr-binding protein VprBP, a WD40 protein associated with the DDB1-CUL4 E3 ubiquitin ligase, is essential for DNA replication and embryonic development. Mol. Cell. Biol. 28, 5621-5633.
24. Nesvizhskii, A. I., Keller, A., Kolker, E. and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658.
25. O'Connell, B. C. and Harper, J. W. (2007). Ubiquitin proteasome system (UPS): what can chromatin do for you? Curr. Opin. Cell Biol. 19, 206-214.
26. Pan, Z. Q., Kentsis, A., Dias, D. C., Yamoah, K. and Wu, K. (2004). Nedd8 on cullin: building an expressway to protein destruction. Oncogene 23, 1985-1997.
27. Petroski, M. D. and Deshaies, R. J. (2005). Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell. Biol. 6, 9-20.
28. Pick, E., Lau, O. S., Tsuge, T., Menon, S., Tong, Y., Dohmae, N., Plafker, S. M., Deng, X. W. and Wei, N. (2007). Mammalian DET1 regulates Cul4A activity and forms stable complexes with E2 ubiquitin-conjugating enzymes. Mol. Cell. Biol. 27, 4708-4719.
29. Pintard, L., Willems, A. and Peter, M. (2004). Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23, 1681-1687.
30. Roshal, M., Kim, B., Zhu, Y., Nghiem, P. and Planelles, V. (2003). Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278, 25879-25886.
31. Sambrook, J., Fristch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Schwechheimer, C., Serino, G., Callis, J., Crosby, W. L., Lyapina, S., Deshaies, R. J., Gray, W. M., Estelle, M. and Deng, X. W. (2001). Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response. Science 292, 1379-1382.
33. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
34. Sumara, I., Quadroni, M., Frei, C., Olma, M. H., Sumara, G., Ricci, R. and Peter, M. (2007). A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev. Cell 12, 887-900.
35. Tomoda, K., Kubota, Y., Arata, Y., Mori, S., Maeda, M., Tanaka, T., Yoshida, M., Yoneda-Kato, N. and Kato, J. Y. (2002). The cytoplasmic shuttling and subsequent degradation of p27Kip1 mediated by Jab1/CSN5 and the COP9 signalosome complex. J. Biol. Chem. 277, 2302-2310.
36. Wee, S., Geyer, R. K., Toda, T. and Wolf, D. A. (2005). CSN facilitates Cullin-RING ubiquitin ligase function by counteracting autocatalytic adapter instability. Nat. Cell Biol. 7, 387-391.
37. Wei, N. and Deng, X. W. (2003). The COP9 signalosome. Annu. Rev. Cell Dev. Biol. 19, 261-286.
38. Willems, A. R., Schwab, M. and Tyers, M. (2004). A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim. Biophys. Acta 1695, 133-170.
39. Wu, J. T., Lin, H. C., Hu, Y. C. and Chien, C. T. (2005). Neddylation and deneddylation regulate Cul1 and Cul3 protein accumulation. Nat. Cell Biol. 7, 1014-1020.
40. Zhang, H. F., Tomida, A., Koshimizu, R., Ogiso, Y., Lei, S. and Tsuruo, T. (2004). Cullin 3 promotes proteasomal degradation of the topoisomerase I-DNA covalent complex. Cancer Res. 64, 1114-1121.