Assembly and structure of Lys33 -linked polyubiquitin reveals distinct conformations

Biochemical Journal

Volumn 467, Issue 2, 2015, Pages 345-352

  Kristariyanto, Yosua Adi ^a   Choi, Soo Youn ^a   Rehman, Syed Arif Abdul ^a   Ritorto, Maria Stella ^a   Campbell, David G ^a   Morrice, Nicholas A ^a,b   Toth, Rachel ^a   Kulathu, Yogesh ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b MDS SCIEX   (Canada)

Author keywords

Deubiquitinase; Homologous to the e6 apc terminus (hect) e3 ligase; Polyubiquitin; Ubiquitin linkage

Indexed keywords

DEUBIQUITINASE; LYSINE; POLYUBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; UBIQUITINATION; ANIMAL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN FOLDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; HUMANS; LYSINE; POLYUBIQUITIN; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN-PROTEIN LIGASES;

EID: 84934971997     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141502     Document Type: Article

References (41)

1. Haglund, K. and Dikic, I. (2005) Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359 CrossRef PubMed
2. Pickart, C.M. and Eddins, M.J. (2004) Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695, 55-72 CrossRef PubMed
3. Deshaies, R.J. and Joazeiro, C.A.P. (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434 CrossRef PubMed
4. Kee, Y. and Huibregtse, J.M. (2007) Regulation of catalytic activities of HECT ubiquitin ligases. Biochem. Biophys. Res. Commun. 354, 329-333 CrossRef PubMed
5. Spratt, D.E., Walden, H. and Shaw, G.S. (2014) RBR E3 ubiquitin ligases: new structures, new insights, new questions. Biochem. J. 458, 421-437 CrossRef PubMed
6. Ikeda, F. and Dikic, I. (2008) Atypical ubiquitin chains: new molecular signals. "Protein modifications: beyond the usual suspects" Review Series. EMBO Rep. 9, 536-542 CrossRef PubMed
7. Kulathu, Y. and Komander, D. (2012) Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 13, 508-523 CrossRef PubMed
8. Virdee, S., Ye, Y., Nguyen, D.P., Komander, D. and Chin, J.W. (2010) Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase. Nat. Chem. Biol. 6, 750-757 CrossRef PubMed
9. Hospenthal, M.K., Freund, S.M. V. and Komander, D. (2013) Assembly, analysis and architecture of atypical ubiquitin chains. Nat. Struct. Mol. Biol. 20, 555-565 CrossRef PubMed
10. Matsumoto, M.L., Wickliffe, K.E., Dong, K.C., Yu, C., Bosanac, I., Bustos, D., Phu, L., Kirkpatrick, D.S., Hymowitz, S.G., Rape, M. et al. (2010) K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 39, 477-484 CrossRef PubMed
11. Bremm, A., Freund, S.M. V. and Komander, D. (2010) Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne. Nat. Struct. Mol. Biol. 17, 939-947 CrossRef PubMed
12. Cook, W.J., Jeffrey, L.C., Carson, M., Chen, Z. and Pickart, C.M. (1992) Structure of a diubiquitin conjugate and a model for interaction with ubiquitin conjugating enzyme (E2). J. Biol. Chem. 267, 16467-16471 PubMed
13. Komander, D., Reyes-Turcu, F., Licchesi, J.D.F., Odenwaelder, P., Wilkinson, K.D. and Barford, D. (2009) Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473 CrossRef PubMed
14. Hirano, T., Serve, O., Yagi-Utsumi, M., Takemoto, E., Hiromoto, T., Satoh, T., Mizushima, T. and Kato, K. (2011) Conformational dynamics of wild-type Lys-48-linked diubiquitin in solution. J. Biol. Chem. 286, 37496-37502 CrossRef PubMed
15. Rohaim, A., Kawasaki, M., Kato, R., Dikic, I. and Wakatsuki, S. (2012) Structure of a compact conformation of linear diubiquitin. Acta Crystallogr. D Biol. Crystallogr. 68, 102-108 CrossRef PubMed
16. Husnjak, K. and Dikic, I. (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322 CrossRef PubMed
17. Chau, V., Tobias, J.W., Bachmair, A., Marriott, D., Ecker, D.J., Gonda, D.K. and Varshavsky, A. (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583 CrossRef PubMed
18. Xu, P., Duong, D.M., Seyfried, N.T., Cheng, D., Xie, Y., Robert, J., Rush, J., Hochstrasser, M., Finley, D. and Peng, J. (2009) Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137, 133-145 CrossRef PubMed
19. Huang, H., Jeon, M.-S., Liao, L., Yang, C., Elly, C., Yates, J.R. and Liu, Y.-C. (2010) K33-linked polyubiquitination of T cell receptor-zeta regulates proteolysis-independent T cell signaling. Immunity 33, 60-70 CrossRef PubMed
20. Al-Hakim, A.K., Zagorska, A., Chapman, L., Deak, M., Peggie, M. and Alessi, D.R. (2008) Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem. J. 411, 249-260 CrossRef PubMed
21. Yuan, W.-C., Lee, Y.-R., Lin, S.-Y., Chang, L.-Y., Tan, Y.P., Hung, C.-C., Kuo, J.-C., Liu, C.-H., Lin, M.-Y., Xu, M. et al. (2014) K33-linked polyubiquitination of coronin 7 by Cul3-KLHL20 ubiquitin e3 ligase regulates protein trafficking. Mol. Cell 54, 586-600 CrossRef PubMed
22. Reyes-Turcu, F.E., Ventii, K.H. and Wilkinson, K.D. (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363-397 CrossRef PubMed
23. Licchesi, J.D. F., Mieszczanek, J., Mevissen, T.E. T., Rutherford, T.J., Akutsu, M., Virdee, S., Oualid, F.E., Chin, J.W., Ovaa, H., Bienz, M. et al. (2011) An ankyrin-repeat ubiquitin-binding domain determines TRABID's specificity for atypical ubiquitin chains. Nat. Struct. Mol. Biol. 19, 62-71 CrossRef PubMed
24. Ritorto, M.S., Ewan, R., Perez-Oliva, A.B., Knebel, A., Buhrlage, S.J., Wightman, M., Kelly, S.M., Wood, N.T., Virdee, S., Gray, N.S. et al. (2014) Screening of DUB activity and specificity by MALDI-TOF mass spectrometry. Nat. Commun. 5, 4763 CrossRef PubMed
25. Tran, H., Hamada, F., Schwarz-Romond, T. and Bienz, M. (2008) Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains. Genes Dev. 22, 528-542 CrossRef PubMed
26. Kulathu, Y., Akutsu, M., Bremm, A., Hofmann, K. and Komander, D. (2009) Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 16, 1328-1330 CrossRef PubMed
27. Stieglitz, B., Morris Davies, A.C., Koliopoulos, M.G., Christodoulou, E. and Rittinger, K. (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 13, 840-846 CrossRef PubMed
28. Kar, G., Keskin, O., Nussinov, R. and Gursoy, A. (2012) Human proteome-scale structural modeling of E2-E3 interactions exploiting interface motifs. J. Proteome Res. 11, 1196-1207 CrossRef PubMed
29. Sheng, Y., Hong, J.H., Doherty, R., Srikumar, T., Shloush, J., Avvakumov, G.V., Walker, J.R., Xue, S., Neculai, D., Wan, J.W. et al. (2012) A human ubiquitin conjugating enzyme (E2)-HECT E3 ligase structure-function screen. Mol. Cell. Proteomics 11, 329-341 CrossRef PubMed
30. Peterson, A.C., Russell, J.D., Bailey, D.J., Westphall, M.S. and Coon, J.J. (2012) Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol. Cell. Proteomics 11, 1475-1488 CrossRef PubMed
31. You, J. and Pickart, C.M. (2001) A HECT domain E3 enzyme assembles novel polyubiquitin chains. J. Biol. Chem. 276, 19871-19878 CrossRef PubMed
32. Maspero, E., Mari, S., Valentini, E., Musacchio, A., Fish, A., Pasqualato, S. and Polo, S. (2011) Structure of the HECT:ubiquitin complex and its role in ubiquitin chain elongation. EMBO Rep. 12, 342-349 CrossRef PubMed
33. Chastagner, P., Israel, A. and Brou, C. (2006) Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep. 7, 1147-1153 CrossRef PubMed
34. Lange, O.F., Lakomek, N.A., Fares, C., Schroder, G.F., Walter, K.F. A., Becker, S., Meiler, J., Grubmuller, H., Griesinger, C. and de Groot, B.L. (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320, 1471-1475 CrossRef PubMed
35. Fushman, D. and Walker, O. (2010) Exploring the linkage dependence of polyubiquitin conformations using molecular modeling. J. Mol. Biol. 395, 803-814 CrossRef PubMed
36. Lai, M.-Y., Zhang, D., LaRonde-LeBlanc, N. and Fushman, D. (2012) Structural and biochemical studies of the open state of Lys48-linked diubiquitin. Biochim. Biophys. Acta 1823, 2046-2056 CrossRef PubMed
37. Varadan, R., Walker, O., Pickart, C. and Fushman, D. (2002) Structural properties of polyubiquitin chains in solution. J. Mol. Biol. 324, 637-647 CrossRef PubMed
38. Kim, J.B., Kim, S.Y., Kim, B.M., Lee, H., Kim, I., Yun, J., Jo, Y., Oh, T., Jo, Y., Chae, H.D. et al. (2013) Identification of a Novel Anti-apoptotic E3 ubiquitin ligase that ubiquitinates antagonists of inhibitor of apoptosis proteins SMAC, HtrA2, and ARTS. J. Biol. Chem. 288, 12014-12021 CrossRef PubMed
39. Emmerich, C.H., Ordureau, A., Strickson, S., Arthur, J.S. C., Pedrioli, P.G. A., Komander, D. and Cohen, P. (2013) Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. U.S.A. 110, 15247-15252 CrossRef PubMed
40. Meyer, H.-J. and Rape, M. (2014) Enhanced protein degradation by branched ubiquitin chains. Cell 157, 910-921 CrossRef PubMed
41. Vijay-Kumar, S., Bugg, C.E. and Cook, W.J. (1987) Structure of ubiquitin refined at 1.8 A resolution. J. Mol. Biol. 194, 531-544 CrossRef PubMed