The proteasome distinguishes between heterotypic and homotypic lysine-11-Linked polyubiquitin chains

Cell Reports

Volumn 12, Issue 4, 2015, Pages 545-553

  Grice, Guinevere L ^a   Lobb, Ian T ^a   Weekes, Michael P ^a,b   Gygi, Steven P ^b   Antrobus, Robin ^a   Nathan, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN B1; LYSINE; POLYUBIQUITIN; PROTEASOME; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME DEGRADATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; UBIQUITINATION; AMINO ACID SEQUENCE; CHEMISTRY; ENZYME SPECIFICITY; HELA CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; CYCLIN B1; HELA CELLS; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; POLYUBIQUITIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; SUBSTRATE SPECIFICITY; UBIQUITINATION;

EID: 84947045877     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.061     Document Type: Article

References (30)

1. Besche, H.C., Haas, W., Gygi, S.P., and Goldberg, A.L. (2009). Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitinlike domain from HHR23B reveals novel proteasome-associated proteins. Biochemistry 48, 2538-2549.
2. Boname, J.M., Thomas, M., Stagg, H.R., Xu, P., Peng, J., and Lehner, P.J. (2010). Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 11, 210-220.
3. Bremm, A., Freund, S.M., 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.
4. Bremm, A., Moniz, S., Mader, J., Rocha, S., and Komander, D. (2014). Cezanne (OTUD7B) regulates HIF-1a homeostasis in a proteasome-independent manner. EMBO Rep. 15, 1268-1277.
5. Castañeda, C.A., Kashyap, T.R., Nakasone, M.A., Krueger, S., and Fushman, D. (2013). Unique structural, dynamical, and functional properties of k11-linked polyubiquitin chains. Structure 21, 1168-1181.
6. Dao, K.H., Rotelli, M.D., Petersen, C.L., Kaech, S., Nelson, W.D., Yates, J.E., Hanlon Newell, A.E., Olson, S.B., Druker, B.J., and Bagby, G.C. (2012). FANCL ubiquitinates b-catenin and enhances its nuclear function. Blood 120, 323-334.
7. Dimova, N.V., Hathaway, N.A., Lee, B.H., Kirkpatrick, D.S., Berkowitz, M.L., Gygi, S.P., Finley, D., and King, R.W. (2012). APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat. Cell Biol. 14, 168-176.
8. Dong, K.C., Helgason, E., Yu, C., Phu, L., Arnott, D.P., Bosanac, I., Compaan, D.M., Huang, O.W., Fedorova, A.V., Kirkpatrick, D.S., et al. (2011). Preparation of distinct ubiquitin chain reagents of high purity and yield. Structure 19, 1053- 1063.
9. Dynek, J.N., Goncharov, T., Dueber, E.C., Fedorova, A.V., Izrael-Tomasevic, A., Phu, L., Helgason, E., Fairbrother, W.J., Deshayes, K., Kirkpatrick, D.S., and Vucic, D. (2010). c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J. 29, 4198-4209.
10. Garnett, M.J., Mansfeld, J., Godwin, C., Matsusaka, T., Wu, J., Russell, P., Pines, J., and Venkitaraman, A.R. (2009). UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nat. Cell Biol. 11, 1363-1369.
11. Husnjak, K., Elsasser, S., Zhang, N., Chen, X., Randles, L., Shi, Y., Hofmann, K., Walters, K.J., Finley, D., and Dikic, I. (2008). Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453, 481-488.
12. 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.
13. Jin, L., Williamson, A., Banerjee, S., Philipp, I., and Rape, M. (2008). Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 133, 653-665.
14. Kim, H.T., Kim, K.P., Uchiki, T., Gygi, S.P., and Goldberg, A.L. (2009). S5a promotes protein degradation by blocking synthesis of nondegradable forked ubiquitin chains. EMBO J. 28, 1867-1877.
15. Kirkpatrick, D.S., Hathaway, N.A., Hanna, J., Elsasser, S., Rush, J., Finley, D., King, R.W., and Gygi, S.P. (2006). Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 8, 700-710.
16. Lee, B.H., Lee, M.J., Park, S., Oh, D.C., Elsasser, S., Chen, P.C., Gartner, C., Dimova, N., Hanna, J., Gygi, S.P., et al. (2010). Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467, 179-184.
17. Lu, Y., Lee, B.H., King, R.W., Finley, D., and Kirschner, M.W. (2015). Substrate degradation by the proteasome: a single-molecule kinetic analysis. Science 348, 1250834.
18. Mansour, W., Nakasone, M.A., von Delbrück, M., Yu, Z., Krutauz, D., Reis, N., Kleifeld, O., Sommer, T., Fushman, D., and Glickman, M.H. (2015). Disassembly of Lys11 and mixed linkage polyubiquitin conjugates provide insights into function of proteasomal deubiquitinases Rpn11 and Ubp6. J. Biol. Chem. 290, 4688-4704.
19. 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.
20. Meyer, H.J., and Rape, M. (2014). Enhanced protein degradation by branched ubiquitin chains. Cell 157, 910-921.
21. Nathan, J.A., Kim, H.T., Ting, L., Gygi, S.P., and Goldberg, A.L. (2013). Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? EMBO J. 32, 552-565.
22. Peth, A., Besche, H.C., and Goldberg, A.L. (2009). Ubiquitinated proteins activate the proteasome by binding to Usp14/Ubp6, which causes 20S gate opening. Mol. Cell 36, 794-804.
23. Peth, A., Uchiki, T., and Goldberg, A.L. (2010). ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 40, 671-681.
24. Prakash, S., Tian, L., Ratliff, K.S., Lehotzky, R.E., and Matouschek, A. (2004). An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11, 830-837.
25. Qin, Y., Zhou, M.T., Hu, M.M., Hu, Y.H., Zhang, J., Guo, L., Zhong, B., and Shu, H.B. (2014). RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog. 10, e1004358.
26. Schreiner, P., Chen, X., Husnjak, K., Randles, L., Zhang, N., Elsasser, S., Finley, D., Dikic, I., Walters, K.J., and Groll, M. (2008). Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453, 548-552.
27. Wickliffe, K.E., Lorenz, S., Wemmer, D.E., Kuriyan, J., and Rape, M. (2011). The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 144, 769-781.
28. Wu, T., Merbl, Y., Huo, Y., Gallop, J.L., Tzur, A., and Kirschner, M.W. (2010). UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 107, 1355-1360.
29. 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.
30. Zhang, Z., Yang, J., Kong, E.H., Chao, W.C., Morris, E.P., da Fonseca, P.C., and Barford, D. (2013). Recombinant expression, reconstitution and structure of human anaphase-promoting complex (APC/C). Biochem. J. 449, 365-371.