Structural Insights into WD-Repeat 48 Activation of Ubiquitin-Specific Protease 46

Structure

Volumn 23, Issue 11, 2015, Pages 2043-2054

  Yin, Jianping ^a   Schoeffler, Allyn J ^a   Wickliffe, Katherine ^a   Newton, Kim ^a   Starovasnik, Melissa A ^a   Dueber, Erin C ^a   Harris, Seth F ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DEUBIQUITINASE; SUMO PROTEIN; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 46; UNCLASSIFIED DRUG; WD REPEAT PROTEIN WDR48; PROTEIN; PROTEIN BINDING; PROTEINASE; UBIQUITIN-SPECIFIC PEPTIDASE 46, HUMAN; WDR48 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; IN VITRO STUDY; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION;

AMINO ACID SEQUENCE; BINDING SITES; ENDOPEPTIDASES; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEINS;

EID: 84946499431     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.08.010     Document Type: Article

References (44)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, and et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. G.V. Avvakumov, J.R. Walker, S. Xue, P.J. Finerty, F. Mackenzie, E.M. Newman, and S. Dhe-Paganon Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8) J. Biol. Chem. 281 2006 38061 38070
3. B. Bingol, J.S. Tea, L. Phu, M. Reichelt, C.E. Bakalarski, Q. Song, O. Foreman, D.S. Kirkpatrick, and M. Sheng The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy Nature 510 2014 370 375
4. G. Bricogne, E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O.S. Smart, C. Vonrhein, and et al. BUSTER Version 2.11.4 2011 Global Phasing Ltd
5. J. Chen, T.S. Dexheimer, Y. Ai, Q. Liang, M.A. Villamil, J. Inglese, D.J. Maloney, A. Jadhav, A. Simeonov, and Z. Zhuang Selective and cell-active inhibitors of the USP1/UAF1 deubiquitinase complex reverse cisplatin resistance in non-small cell lung cancer cells Chem. Biol. 18 2011 1390 1400
6. M.A. Cohn, P. Kowal, K. Yang, W. Haas, T.T. Huang, S.P. Gygi, and A.D. D'Andrea A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway Mol. Cell 28 2007 786 797
7. M.A. Cohn, Y. Kee, W. Haas, S.P. Gygi, and A.D. D'Andrea UAF1 is a subunit of multiple deubiquitinating enzyme complexes J. Biol. Chem. 284 2009 5343 5351
8. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
9. A.C. Faesen, A.M.G. Dirac, A. Shanmugham, H. Ovaa, A. Perrakis, and T.K. Sixma Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase Mol. Cell 44 2011 147 159
10. A.C. Faesen, M.P.A. Luna-Vargas, P.P. Geurink, M. Clerici, R. Merkx, W.J. van Dijk, D.S. Hameed, F. El Oualid, H. Ovaa, and T.K. Sixma The differential modulation of USP activity by internal regulatory domains, interactors and eight ubiquitin chain types Chem. Biol. 18 2011 1550 1561
11. N.R. Gangula, and S. Maddika WD repeat protein WDR48 in complex with deubiquitinase USP12 suppresses Akt-dependent cell survival signaling by stabilizing PH domain leucine-rich repeat protein phosphatase 1 (PHLPP1) J. Biol. Chem. 288 2013 34545 34554
12. I. García-Santisteban, K. Zorroza, and J.A. Rodríguez Two nuclear localization signals in USP1 mediate nuclear import of the USP1/UAF1 complex PLoS One 7 2012 e38570
13. I. García-Santisteban, G.J. Peters, E. Giovannetti, and J.A. Rodríguez USP1 deubiquitinase: cellular functions, regulatory mechanisms and emerging potential as target in cancer therapy Mol. Cancer 12 2013 91
14. A. Hershko, E. Eytan, A. Ciechanover, and A.L. Haas Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins J. Biol. Chem. 257 1982 13964 13970
15. L. Holm, and C. Sander Dali: a network tool for protein structure comparison Trends Biochem. Sci. 20 1995 478 480
16. M. Hu, P. Li, M. Li, W. Li, T. Yao, J.-W. Wu, W. Gu, R.E. Cohen, and Y. Shi Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde Cell 111 2002 1041 1054
17. M. Hu, P. Li, L. Song, P.D. Jeffrey, T.A. Chenova, K.D. Wilkinson, R.E. Cohen, and Y. Shi Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14 EMBO J. 24 2005 3747 3756
18. T.T. Huang, S.M.B. Nijman, K.D. Mirchandani, P.J. Galardy, M.A. Cohn, W. Haas, S.P. Gygi, H.L. Ploegh, R. Bernards, and A.D. D'Andrea Regulation of monoubiquitinated PCNA by DUB autocleavage Nat. Cell Biol. 8 2006 339 347
19. O.W. Huang, X. Ma, J. Yin, J. Flinders, T. Maurer, N. Kayagaki, Q. Phung, I. Bosanac, D. Arnott, V.M. Dixit, and et al. Phosphorylation-dependent activity of the deubiquitinase DUBA Nat. Struct. Mol. Biol. 19 2012 171 175
20. H.-Y. Joo, A. Jones, C. Yang, L. Zhai, A.D. Smith, Z. Zhang, M.B. Chandrasekharan, Z.-W. Sun, M.B. Renfrow, Y. Wang, and et al. Regulation of histone H2A and H2B deubiquitination and Xenopus development by USP12 and USP46 J. Biol. Chem. 286 2011 7190 7201
21. Y. Kee, K. Yang, M.A. Cohn, W. Haas, S.P. Gygi, and A.D. D'Andrea WDR20 regulates activity of the USP12 x UAF1 deubiquitinating enzyme complex J. Biol. Chem. 285 2010 11252 11257
22. A. Köhler, E. Zimmerman, M. Schneider, E. Hurt, and N. Zheng Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module Cell 141 2010 606 617
23. D. Komander, and M. Rape The ubiquitin code Annu. Rev. Biochem. 81 2012 203 229
24. D. Komander, M.J. Clague, and S. Urbé Breaking the chains: structure and function of the deubiquitinases Nat. Rev. Mol. Cell Biol. 10 2009 550 563
25. M. Lehoux, D. Gagnon, and J. Archambault E1-mediated recruitment of a UAF1-USP deubiquitinase complex facilitates human papillomavirus DNA replication J. Virol. 88 2014 8545 8555
26. Q. Liang, T.S. Dexheimer, P. Zhang, A.S. Rosenthal, M.A. Villamil, C. You, Q. Zhang, J. Chen, C.A. Ott, H. Sun, and et al. A selective USP1-UAF1 inhibitor links deubiquitination to DNA damage responses Nat. Chem. Biol. 10 2014 298 304
27. U.L. McClurg, E.E. Summerscales, V.J. Harle, L. Gaughan, and C.N. Robson Deubiquitinating enzyme Usp12 regulates the interaction between the androgen receptor and the Akt pathway Oncotarget 5 2014 7081 7092
28. K. Molland, Q. Zhou, and A.D. Mesecar A 2.2 Å resolution structure of the USP7 catalytic domain in a new space group elaborates upon structural rearrangements resulting from ubiquitin binding Acta Crystallogr. F Struct. Biol. Commun. 70 2014 283 287
29. J. Murai, K. Yang, D. Dejsuphong, K. Hirota, S. Takeda, and A.D. D'Andrea The USP1/UAF1 complex promotes double-strand break repair through homologous recombination Mol. Cell. Biol. 31 2011 2462 2469
30. S.M.B. Nijman, T.T. Huang, A.M.G. Dirac, T.R. Brummelkamp, R.M. Kerkhoven, A.D. D'Andrea, and R. Bernards The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway Mol. Cell 17 2005 331 339
31. A. Olazabal-Herrero, I. García-Santisteban, and J. Rodríguez Structure-function analysis of USP1: insights into the role of Ser313 phosphorylation site and the effect of cancer-associated mutations on autocleavage Mol. Cancer 14 2015 33
32. E. Park, J.M. Kim, B. Primack, D.M. Weinstock, L.A. Moreau, K. Parmar, and A.D. D'Andrea Inactivation of Uaf1 causes defective homologous recombination and early embryonic lethality in mice Mol. Cell. Biol. 33 2013 4360 4370
33. F.E. Reyes-Turcu, and K.D. Wilkinson Polyubiquitin binding and disassembly by deubiquitinating enzymes Chem. Rev. 109 2009 1495 1508
34. N.L. Samara, A.B. Datta, C.E. Berndsen, X. Zhang, T. Yao, R.E. Cohen, and C. Wolberger Structural insights into the assembly and function of the SAGA deubiquitinating module Science 328 2010 1025 1029
35. M.E. Sowa, E.J. Bennett, S.P. Gygi, and J.W. Harper Defining the human deubiquitinating enzyme interaction landscape Cell 138 2009 389 403
36. L.K. Teixeira, and S.I. Reed Ubiquitin ligases and cell cycle control Annu. Rev. Biochem. 82 2013 387 414
37. T.C. Terwilliger, P.D. Adams, R.J. Read, A.J. McCoy, N.W. Moriarty, R.W. Grosse-Kunstleve, P.V. Afonine, P.H. Zwart, and L.-W. Hung Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Acta Crystallogr. D Biol. Crystallogr. 65 2009 582 601
38. M.A. Villamil, J. Chen, Q. Liang, and Z. Zhuang A noncanonical cysteine protease USP1 is activated through active site modulation by USP1-associated factor 1 Biochemistry 51 2012 2829 2839
39. M.A. Villamil, Q. Liang, J. Chen, Y.S. Choi, S. Hou, K.H. Lee, and Z. Zhuang Serine phosphorylation is critical for the activation of ubiquitin-specific protease 1 and its interaction with WD40-repeat protein UAF1 Biochemistry 51 2012 9112 9123
40. M.A. Villamil, Q. Liang, and Z. Zhuang The WD40-repeat protein-containing deubiquitinase complex: catalysis, regulation, and potential for therapeutic intervention Cell Biochem. Biophys. 67 2013 111 126
41. S.A. Williams, H.L. Maecker, D.M. French, J. Liu, A. Gregg, L.B. Silverstein, T.C. Cao, R.A.D. Carano, and V.M. Dixit USP1 deubiquitinates ID proteins to preserve a mesenchymal stem cell program in osteosarcoma Cell 146 2011 918 930
42. C. Xu, and J. Min Structure and function of WD40 domain proteins Protein Cell 2 2011 202 214
43. K. Yang, G.-L. Moldovan, P. Vinciguerra, J. Murai, S. Takeda, and A.D. D'Andrea Regulation of the Fanconi anemia pathway by a SUMO-like delivery network Genes Dev. 25 2011 1847 1858
44. Y. Ye, H. Scheel, K. Hofmann, and D. Komander Dissection of USP catalytic domains reveals five common insertion points Mol. Biosyst. 5 2009 1797 1808