Discovery of specific inhibitors of human USP7/HAUSP deubiquitinating enzyme

Chemistry and Biology

Volumn 19, Issue 4, 2012, Pages 467-477

  Reverdy, Céline ^a   Conrath, Susan ^a   Lopez, Roman ^a   Planquette, Cécile ^a   Atmanene, Cédric ^b   Collura, Vincent ^a   Harpon, Jane ^a   Battaglia, Véronique ^a   Vivat, Valérie ^b   Sippl, Wolfgang ^c   Colland, Frédéric ^a  

^a Hybrigenics SA   (France)

^b NovAliX   (France)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; UNCLASSIFIED DRUG; USP7 DEUBIQUITINATING ENZYME INHIBITOR;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG SCREENING; DRUG SELECTIVITY; HUMAN; HUMAN CELL; RECEPTOR OCCUPANCY; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; G1 PHASE CELL CYCLE CHECKPOINTS; HCT116 CELLS; HUMANS; SMALL MOLECULE LIBRARIES; UBIQUITIN THIOLESTERASE;

EID: 84860112066     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.02.007     Document Type: Article

References (37)

1. M. Altun, H.B. Kramer, L.I. Willems, J.L. McDermott, C.A. Leach, S.J. Goldenberg, K.G. Kumar, R. Konietzny, R. Fischer, and E. Kogan Activity-based chemical proteomics accelerates inhibitor development for deubiquitylating enzymes Chem. Biol. 18 2011 1401 1412
2. K. Becker, N.D. Marchenko, G. Palacios, and U.M. Moll A role of HAUSP in tumor suppression in a human colon carcinoma xenograft model Cell Cycle 7 2008 7 10
3. A. Borodovsky, H. Ovaa, N. Kolli, T. Gan-Erdene, K.D. Wilkinson, H.L. Ploegh, and B.M. Kessler Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family Chem. Biol. 9 2002 1149 1159
4. J.W. Chang, D.K. Nomura, and B.F. Cravatt A potent and selective inhibitor of KIAA1363/AADACL1 that impairs prostate cancer pathogenesis Chem. Biol. 18 2011 476 484
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. P. Cohen, and M. Tcherpakov Will the ubiquitin system furnish as many drug targets as protein kinases? Cell 143 2010 686 693
7. F. Colland, E. Formstecher, X. Jacq, C. Reverdy, C. Planquette, S. Conrath, V. Trouplin, J. Bianchi, V.N. Aushev, and J. Camonis Small-molecule inhibitor of USP7/HAUSP ubiquitin protease stabilizes and activates p53 in cells Mol. Cancer Ther. 8 2009 2286 2295
8. F. Colland The therapeutic potential of deubiquitinating enzyme inhibitors Biochem. Soc. Trans. 38 2010 137 143
9. J.M. Cummins, C. Rago, M. Kohli, K.W. Kinzler, C. Lengauer, and B. Vogelstein Tumour suppression: disruption of HAUSP gene stabilizes p53 Nature 428 2004 10.1038/nature02501
10. L.C. Dang, F.D. Melandri, and R.L. Stein Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes Biochemistry 37 1998 1868 1879
11. M. Drag, and G.S. Salvesen Emerging principles in protease-based drug discovery Nat. Rev. Drug Discov. 9 2010 690 701
12. M. Drag, J. Mikolajczyk, M. Bekes, F.E. Reyes-Turcu, J.A. Ellman, K.D. Wilkinson, and G.S. Salvesen Positional-scanning fluorigenic substrate libraries reveal unexpected specificity determinants of DUBs (deubiquitinating enzymes) Biochem. J. 415 2008 367 375
13. Z. Du, J. Song, Y. Wang, Y. Zhao, K. Guda, S. Yang, H.Y. Kao, Y. Xu, J. Willis, and S.D. Markowitz DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation-driven ubiquitination Sci. Signal. 3 2010 ra80
14. M.T. Epping, L.A. Meijer, O. Krijgsman, J.L. Bos, P.P. Pandolfi, and R. Bernards TSPYL5 suppresses p53 levels and function by physical interaction with USP7 Nat. Cell Biol. 13 2011 102 108
15. R.D. Everett, M. Meredith, and A. Orr The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication J. Virol. 73 1999 417 426
16. A.C. Faesen, A.M. 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
17. H. Faustrup, S. Bekker-Jensen, J. Bartek, J. Lukas, and N. Mailand USP7 counteracts SCFbetaTrCP- but not APCCdh1-mediated proteolysis of Claspin J. Cell Biol. 184 2009 13 19
18. J. Hemelaar, A. Borodovsky, B.M. Kessler, D. Reverter, J. Cook, N. Kolli, T. Gan-Erdene, K.D. Wilkinson, G. Gill, and C.D. Lima Specific and covalent targeting of conjugating and deconjugating enzymes of ubiquitin-like proteins Mol. Cell. Biol. 24 2004 84 95
19. 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
20. 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
21. B.H. Lee, M.J. Lee, S. Park, D.C. Oh, S. Elsasser, P.C. Chen, C. Gartner, N. Dimova, J. Hanna, and S.P. Gygi Enhancement of proteasome activity by a small-molecule inhibitor of USP14 Nature 467 2010 179 184
22. M. Li, C.L. Brooks, N. Kon, and W. Gu A dynamic role of HAUSP in the p53-Mdm2 pathway Mol. Cell 13 2004 879 886
23. G.N. Maertens, S. El Messaoudi-Aubert, S. Elderkin, K. Hiom, and G. Peters Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor EMBO J. 29 2010 2553 2565
24. A. Monge, A. Arrault, C. Marot, and L. Morin-Allory Managing, profiling and analyzing a library of 2.6 million compounds gathered from 32 chemical providers Mol. Divers. 10 2006 389 403
25. M. Muratani, D. Gerlich, S.M. Janicki, M. Gebhard, R. Eils, and D.L. Spector Metabolic-energy-dependent movement of PML bodies within the mammalian cell nucleus Nat. Cell Biol. 4 2002 106 110
26. S.M. Nijman, M.P. Luna-Vargas, A. Velds, T.R. Brummelkamp, A.M. Dirac, T.K. Sixma, and R. Bernards A genomic and functional inventory of deubiquitinating enzymes Cell 123 2005 773 786
27. H. Ovaa, B.M. Kessler, U. Rolén, P.J. Galardy, H.L. Ploegh, and M.G. Masucci Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells Proc. Natl. Acad. Sci. USA 101 2004 2253 2258
28. M.P. Patricelli, T.K. Nomanbhoy, J. Wu, H. Brown, D. Zhou, J. Zhang, S. Jagannathan, A. Aban, E. Okerberg, and C. Herring In situ kinase profiling reveals functionally relevant properties of native kinases Chem. Biol. 18 2011 699 710
29. K. Ratia, S. Pegan, J. Takayama, K. Sleeman, M. Coughlin, S. Baliji, R. Chaudhuri, W. Fu, B.S. Prabhakar, and M.E. Johnson A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication Proc. Natl. Acad. Sci. USA 105 2008 16119 16124
30. W. Sippl, V. Collura, and F. Colland Ubiquitin-specific proteases as cancer drug targets Future Oncol. 7 2011 619 632
31. M.S. Song, L. Salmena, A. Carracedo, A. Egia, F. Lo-Coco, J. Teruya-Feldstein, and P.P. Pandolfi The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network Nature 455 2008 813 817
32. A. van der Horst, A.M. de Vries-Smits, A.B. Brenkman, M.H. van Triest, N. van den Broek, F. Colland, M.M. Maurice, and B.M. Burgering FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP Nat. Cell Biol. 8 2006 1064 1073
33. L.T. Vassilev, B.T. Vu, B. Graves, D. Carvajal, F. Podlaski, Z. Filipovic, N. Kong, U. Kammlott, C. Lukacs, and C. Klein In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848
34. V. Vivat Hannah, C. Atmanene, D. Zeyer, A. Van Dorsselaer, and S. Sanglier-Cianférani Native MS: an 'ESI' way to support structure- and fragment-based drug discovery Future Med. Chem 2 2010 35 50
35. Y. Yang, R.L. Ludwig, J.P. Jensen, S.A. Pierre, M.V. Medaglia, I.V. Davydov, Y.J. Safiran, P. Oberoi, J.H. Kenten, and A.C. Phillips Small molecule inhibitors of HDM2 ubiquitin ligase activity stabilize and activate p53 in cells Cancer Cell 7 2005 547 559
36. J.M. Zapata, K. Pawlowski, E. Haas, C.F. Ware, A. Godzik, and J.C. Reed A diverse family of proteins containing tumor necrosis factor receptor-associated factor domains J. Biol. Chem. 276 2001 24242 24252
37. J.H. Zhang, T.D. Chung, and K.R. Oldenburg A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73