Selective and cell-active inhibitors of the USP1/ UAF1 deubiquitinase complex reverse cisplatin resistance in non-small cell lung cancer cells

Chemistry and Biology

Volumn 18, Issue 11, 2011, Pages 1390-1400

  Chen, Junjun ^a   Dexheimer, Thomas S ^b   Ai, Yongxing ^a   Liang, Qin ^a   Villamil, Mark A ^a   Inglese, James ^b   Maloney, David J ^b   Jadhav, Ajit ^b   Simeonov, Anton ^b   Zhuang, Zhihao ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [4 [2 [3 CYCLOHEXYL 1 (4 CYCLOHEXYLBUTYL)UREIDO]ETHYL]PHENYLTHIO] 2 METHYLPROPIONIC ACID; ANTINEOPLASTIC AGENT; BUTYRIC ACID DERIVATIVE; CARBANILAMIDE DERIVATIVE; CISPLATIN; NUCLEAR PROTEIN; PIMOZIDE; PROTEINASE; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE; UBIQUITIN-SPECIFIC PROTEASE; USP1 ASSOCIATED FACTOR 1, HUMAN;

ARTICLE; CELL PROLIFERATION; CHEMISTRY; DNA REPAIR; DRUG ANTAGONISM; DRUG RESISTANCE; ENZYMOLOGY; FANCONI ANEMIA; HUMAN; KINETICS; LUNG NON SMALL CELL CANCER; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BUTYRIC ACIDS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; ENDOPEPTIDASES; FANCONI ANEMIA; HUMANS; KINETICS; NUCLEAR PROTEINS; PHENYLUREA COMPOUNDS; PIMOZIDE; UBIQUITIN;

EID: 82255194029     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2011.08.014     Document Type: Article

References (56)

1. J. Adams The proteasome: a suitable antineoplastic target Nat. Rev. Cancer 4 2004 349 360 (Pubitemid 38579481)
2. M.R. Albertella, C.M. Green, A.R. Lehmann, and M.J. O'Connor A role for polymerase eta in the cellular tolerance to cisplatin-induced damage Cancer Res. 65 2005 9799 9806 (Pubitemid 41541457)
3. A.F. Alpi, and K.J. Patel Monoubiquitylation in the Fanconi anemia DNA damage response pathway DNA Repair (Amst.) 8 2009 430 435
4. A.Y. Amerik, and M. Hochstrasser Mechanism and function of deubiquitinating enzymes Biochim. Biophys. Acta 1695 2004 189 207 (Pubitemid 39574973)
5. A.Y. Amerik, S. Swaminathan, B.A. Krantz, K.D. Wilkinson, and M. Hochstrasser In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome EMBO J. 16 1997 4826 4838 (Pubitemid 27348392)
6. S. Bergink, and S. Jentsch Principles of ubiquitin and SUMO modifications in DNA repair Nature 458 2009 461 467
7. A. Bremm, S.M. Freund, and D. Komander Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne Nat. Struct. Mol. Biol. 17 2010 939 947
8. P.J. Brown, L.W. Stuart, K.P. Hurley, M.C. Lewis, D.A. Winegar, J.G. Wilson, W.O. Wilkison, O.R. Ittoop, and T.M. Willson Identification of a subtype selective human PPARalpha agonist through parallel-array synthesis Bioorg. Med. Chem. Lett. 11 2001 1225 1227 (Pubitemid 32406090)
9. J. Brun, R.K. Chiu, B.G. Wouters, and D.A. Gray Regulation of PCNA polyubiquitination in human cells BMC Res. Notes 3 2010 85
10. T.C. Chou Drug combination studies and their synergy quantification using the Chou-Talalay method Cancer Res. 70 2010 440 446
11. T.C. Chou, and P. Talalay Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors Adv. Enzyme Regul. 22 1984 27 55
12. T.C. Chou, R.J. Motzer, Y. Tong, and G.J. Bosl Computerized quantitation of synergism and antagonism of taxol, topotecan, and cisplatin against human teratocarcinoma cell growth: a rational approach to clinical protocol design J. Natl. Cancer Inst. 86 1994 1517 1524 (Pubitemid 24330215)
13. 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
14. 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 (Pubitemid 350217060)
15. 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
16. E.M. Cooper, J.D. Boeke, and R.E. Cohen Specificity of the BRISC deubiquitinating enzyme is not due to selective binding to Lys63-linked polyubiquitin J. Biol. Chem. 285 2010 10344 10352
17. R.A. Copeland Evaluation of enzyme inhibitors in drug discovery a guide for medicinal chemists and pharmacologists Methods of biochemical analysis v 46 2005 Wiley-Interscience Hoboken, NJ 125 128
18. M. Drag, and G.S. Salvesen Emerging principles in protease-based drug discovery Nat. Rev. Drug Discov. 9 2010 690 701
19. L. Geng, C.J. Huntoon, and L.M. Karnitz RAD18-mediated ubiquitination of PCNA activates the Fanconi anemia DNA repair network J. Cell Biol. 191 2010 249 257
20. P. Guédat, and F. Colland Patented small molecule inhibitors in the ubiquitin proteasome system BMC Biochem. 8 Suppl 1 2007 S14
21. U. Hassiepen, U. Eidhoff, G. Meder, J.F. Bulber, A. Hein, U. Bodendorf, E. Lorthiois, and B. Martoglio A sensitive fluorescence intensity assay for deubiquitinating proteases using ubiquitin-rhodamine110-glycine as substrate Anal. Biochem. 371 2007 201 207 (Pubitemid 350015966)
22. J.K. Hicks, C.L. Chute, M.T. Paulsen, R.L. Ragland, N.G. Howlett, Q. Guéranger, T.W. Glover, and C.E. Canman Differential roles for DNA polymerases eta, zeta, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links Mol. Cell. Biol. 30 2010 1217 1230
23. T.T. Huang, S.M. 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
24. J. Inglese, D.S. Auld, A. Jadhav, R.L. Johnson, A. Simeonov, A. Yasgar, W. Zheng, and C.P. Austin Quantitative high-throughput screening: a titration-based approach that efficiently identifies biological activities in large chemical libraries Proc. Natl. Acad. Sci. USA 103 2006 11473 11478 (Pubitemid 44182476)
25. P.L. Kannouche, J. Wing, and A.R. Lehmann Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage Mol. Cell 14 2004 491 500 (Pubitemid 38648802)
26. J.M. Kim, K. Parmar, M. Huang, D.M. Weinstock, C.A. Ruit, J.L. Kutok, and A.D. D'Andrea Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype Dev. Cell 16 2009 314 320
27. V. Kirkin, and I. Dikic Role of ubiquitin- and Ubl-binding proteins in cell signaling Curr. Opin. Cell Biol. 19 2007 199 205 (Pubitemid 46386400)
28. A.F. Kisselev, and A.L. Goldberg Proteasome inhibitors: from research tools to drug candidates Chem. Biol. 8 2001 739 758 (Pubitemid 32752454)
29. M.G. Kornacker, Z. Lai, M. Witmer, J. Ma, J. Hendrick, V.G. Lee, D.J. Riexinger, C. Mapelli, W. Metzler, and R.A. Copeland An inhibitor binding pocket distinct from the catalytic active site on human beta-APP cleaving enzyme Biochemistry 44 2005 11567 11573 (Pubitemid 41209092)
30. 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
31. S.L. McGovern, B.T. Helfand, B. Feng, and B.K. Shoichet A specific mechanism of nonspecific inhibition J. Med. Chem. 46 2003 4265 4272 (Pubitemid 37153008)
32. J.P. Neifeld, D.C. Tormey, M.A. Baker, F.L. Meyskens Jr. , and R.N. Taub Phase II trial of the dopaminergic inhibitor pimozide in previously treated melanoma patients Cancer Treat. Rep. 67 1983 155 157 (Pubitemid 13110648)
33. S.M. Nijman, T.T. Huang, A.M. 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 (Pubitemid 40193305)
34. 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 (Pubitemid 41721026)
35. V.H. Oestergaard, F. Langevin, H.J. Kuiken, P. Pace, W. Niedzwiedz, L.J. Simpson, M. Ohzeki, M. Takata, J.E. Sale, and K.J. Patel Deubiquitination of FANCD2 is required for DNA crosslink repair Mol. Cell 28 2007 798 809 (Pubitemid 350217050)
36. L.A. Opler, and S.S. Feinberg The role of pimozide in clinical psychiatry: a review J. Clin. Psychiatry 52 1991 221 233
37. K.J. Patel, and H. Joenje Fanconi anemia and DNA replication repair DNA Repair (Amst.) 6 2007 885 890 (Pubitemid 46880469)
38. A. Radujkovic, M. Schad, J. Topaly, M.R. Veldwijk, S. Laufs, B.S. Schultheis, A. Jauch, J.V. Melo, S. Fruehauf, and W.J. Zeller Synergistic activity of imatinib and 17-AAG in imatinib-resistant CML cells overexpressing BCR-ABL - inhibition of P-glycoprotein function by 17-AAG Leukemia 19 2005 1198 1206 (Pubitemid 40946004)
39. F.E. Reyes-Turcu, K.H. Ventii, and K.D. Wilkinson Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes Annu. Rev. Biochem. 78 2009 363 397
40. Y. Sato, A. Yoshikawa, A. Yamagata, H. Mimura, M. Yamashita, K. Ookata, O. Nureki, K. Iwai, M. Komada, and S. Fukai Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains Nature 455 2008 358 362
41. J.M. Scheer, M.J. Romanowski, and J.A. Wells A common allosteric site and mechanism in caspases Proc. Natl. Acad. Sci. USA 103 2006 7595 7600
42. R.H. Shanks, D.A. Rizzieri, J.L. Flowers, O.M. Colvin, and D.J. Adams Preclinical evaluation of gemcitabine combination regimens for application in acute myeloid leukemia Clin. Cancer Res. 11 2005 4225 4233 (Pubitemid 40791589)
43. A. Simeonov, A. Jadhav, C.J. Thomas, Y. Wang, R. Huang, N.T. Southall, P. Shinn, J. Smith, C.P. Austin, D.S. Auld, and J. Inglese Fluorescence spectroscopic profiling of compound libraries J. Med. Chem. 51 2008 2363 2371 (Pubitemid 351628498)
44. E. Sonoda, T. Okada, G.Y. Zhao, S. Tateishi, K. Araki, M. Yamaizumi, T. Yagi, N.S. Verkaik, D.C. van Gent, M. Takata, and S. Takeda Multiple roles of Rev3, the catalytic subunit of polzeta in maintaining genome stability in vertebrates EMBO J. 22 2003 3188 3197 (Pubitemid 36758638)
45. N.T. Southall, A. Jadhav, R. Huang, T. Nguyen, and Y. Wang Enabling the large-scale analysis of quantitative high-throughput screening data. handbook of drug screening R. Seethala, L. Zhang, Handbook of Drug Screening 2nd ed. 2009 Informa Healthcare New York 442 464
46. 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
47. J.S. Strobl, K.L. Kirkwood, T.K. Lantz, M.A. Lewine, V.A. Peterson, and J.F. Worley 3rd Inhibition of human breast cancer cell proliferation in tissue culture by the neuroleptic agents pimozide and thioridazine Cancer Res. 50 1990 5399 5405 (Pubitemid 20302995)
48. K. Terai, T. Abbas, A.A. Jazaeri, and A. Dutta CRL4(Cdt2) E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis Mol. Cell 37 2010 143 149
49. X. Tian, N.S. Isamiddinova, R.J. Peroutka, S.J. Goldenberg, M.R. Mattern, B. Nicholson, and C. Leach Characterization of selective ubiquitin and ubiquitin-like protease inhibitors using a fluorescence-based multiplex assay format Assay Drug Dev. Technol. 9 2011 165 173
50. S. Virdee, Y. Ye, D.P. Nguyen, D. Komander, and J.W. Chin Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase Nat. Chem. Biol. 6 2010 750 757
51. W. Wang Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins Nat. Rev. Genet. 8 2007 735 748 (Pubitemid 47429206)
52. F. Wu, X. Lin, T. Okuda, and S.B. Howell DNA polymerase zeta regulates cisplatin cytotoxicity, mutagenicity, and the rate of development of cisplatin resistance Cancer Res. 64 2004 8029 8035 (Pubitemid 39446939)
53. J. Zastre, M. Anantha, E. Ramsay, and M. Bally Irinotecan-cisplatin interactions assessed in cell-based screening assays: cytotoxicity, drug accumulation and DNA adduct formation in an NSCLC cell line Cancer Chemother. Pharmacol. 60 2007 91 102 (Pubitemid 46643722)
54. N. Zeng-Rong, J. Paterson, L. Alpert, M.S. Tsao, J. Viallet, and M.A. Alaoui-Jamali Elevated DNA repair capacity is associated with intrinsic resistance of lung cancer to chemotherapy Cancer Res. 55 1995 4760 4764
55. 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 (Pubitemid 29278954)
56. Z. Zhuang, R.E. Johnson, L. Haracska, L. Prakash, S. Prakash, and S.J. Benkovic Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme Proc. Natl. Acad. Sci. USA 105 2008 5361 5366 (Pubitemid 351753868)