Drug discovery and assay development in the ubiquitin-proteasome system

Biochemical Society Transactions

Volumn 38, Issue 1, 2010, Pages 14-20

  Berkers, Celia R ^a   Ovaa, Huib ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Bortezomib; Carfilzomib; Immunoproteasome inhibitor; Mycobactericidal proteasome inhibitor; Proteasome; Proteasome activity assay

Indexed keywords

1,3,4 OXATHIAZOL 2 ONE; ARYGYRIN A; BORTEZOMIB; CARFILZOMIB; CEP 18770; DOXORUBICIN; HISTONE DEACETYLASE INHIBITOR; HT 1171; MLN 4924; NEDD8 PROTEIN; PR 957; PROTEASOME; PROTEASOME INHIBITOR; SALINOSPORAMIDE A; UBIQUITIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERICIDAL ACTIVITY; CANCER INHIBITION; CANCER RESISTANCE; CLINICAL TRIAL; CONFOCAL MICROSCOPY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG SCREENING; DRUG SPECIFICITY; DRUG STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GASTROINTESTINAL SYMPTOM; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC SYSTEM TUMOR; HUMAN; MANTLE CELL LYMPHOMA; MULTIPLE MYELOMA; MYCOBACTERIUM TUBERCULOSIS; NEUROTOXICITY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SOLID TUMOR; UNSPECIFIED SIDE EFFECT;

ANTINEOPLASTIC AGENTS; BIOLOGICAL ASSAY; BORONIC ACIDS; DRUG DISCOVERY; DRUG RESISTANCE, NEOPLASM; MOLECULAR STRUCTURE; NEOPLASMS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; UBIQUITIN;

EID: 76449103616     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0380014     Document Type: Article

References (47)

1. Adams, J. (2004) The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5, 417-421
2. Nalepa, G., Rolfe, M. and Harper, J.W. (2006) Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discov. 5, 596-613
3. Pickart, C.M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
4. Dahlmann, B., Ruppert, T., Kuehn, L., Merforth, S. and Kloetzel, P.M. (2000) Different proteasome subtypes in a single tissue exhibit different enzymatic properties. J. Mol. Biol. 303, 643-653
5. Dahlmann, B., Ruppert, T., Kloetzel, P.M. and Kuehn, L. (2001) Subtypes of 20S proteasomes from skeletal muscle. Biochimie 83, 295-299
6. Chauhan, D., Bianchi, G. and Anderson, K.C. (2008) Targeting the UPS as therapy in multiple myeloma. BMC Biochem. 9, (Suppl. 1), S1
7. Hideshima, T., Richardson, P., Chauhan, D., Palombella, V.J., Elliott, P.J., Adams, J. and Anderson, K.C. (2001) The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 61, 3071-3076
8. Richardson, P.G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S.V., Srkalovic, G., Alsina, M., Alexanian, R. et al. (2003) A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 348, 2609-2617
9. Orlowski, R.Z. and Kuhn, D.J. (2008) Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14, 1649-1657
10. Demo, S.D., Kirk, C.J., Aujay, M.A., Buchholz, T.J., Dajee, M., Ho, M.N., Jiang, J., Laidig, G.J., Lewis, E.R., Parlati, F. et al. (2007) Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Res. 67, 6383-6391
11. Kuhn, D.J., Chen, Q., Voorhees, P.M., Strader, J.S., Shenk, K.D., Sun, C.M., Demo, S.D., Bennett, M.K., van Leeuwen, F.W., Chanan-Khan, A.A. and Orlowski, R.Z. (2007) Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 110, 3281-3290
12. Chauhan, D., Catley, L., Li, G., Podar, K., Hideshima, T., Velankar, M., Mitsiades, C., Mitsiades, N., Yasui, H., Letai, A. et al. (2005) A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell 8, 407-419
13. Dorsey, B.D., Iqbal, M., Chatterjee, S., Menta, E., Bernardini, R., Bernareggi, A., Cassara, P.G., D'Arasmo, G., Ferretti, E., De Munari, S. et al. (2008) Discovery of a potent, selective, and orally active proteasome inhibitor for the treatment of cancer. J. Med. Chem. 51, 1068-1072
14. Piva, R., Ruggeri, B., Williams, M., Costa, G., Tamagno, I., Ferrero, D., Giai, V., Coscia, M., Peola, S., Massaia, M. et al. (2008) CEP-18770: A novel, orally active proteasome inhibitor with a tumor-selective pharmacologic profile competitive with bortezomib. Blood 111, 2765-2775
15. Groll, M., Heinemeyer, W., Jager, S., Ullrich, T., Bochtler, M., Wolf, D.H. and Huber, R. (1999) The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc. Natl. Acad. Sci. U.S.A. 96, 10976-10983
16. Groll, M., Berkers, C.R., Ploegh, H.L. and Ovaa, H. (2006) Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure 14, 451-456
17. Groll, M., Kim, K.B., Kairies, N., Huber, R. and Crews, C.M. (2000) Crystal structure of epoxomicin: 20S proteasome reveals a molecular basis for selectivity of α',β'-epoxyketone proteasome inhibitors. J. Am. Chem. Soc. 122, 1237-1238
18. Groll, M., Huber, R. and Potts, B.C. (2006) Crystal structures of Salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of β-lactone ring opening and a mechanism for irreversible binding. J. Am. Chem. Soc. 128, 5136-5141
19. Berkers, C.R., Verdoes, M., Lichtman, E., Fiebiger, E., Kessler, B.M., Anderson, K.C., Ploegh, H.L., Ovaa, H. and Galardy, P.J. (2005) Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat. Methods 2, 357-362
20. Stapnes, C., Doskeland, A.P., Hatfield, K., Ersvaer, E., Ryningen, A., Lorens, J.B., Gjertsen, B.T. and Bruserud, O. (2007) The proteasome inhibitors bortezomib and PR-171 have antiproliferative and proapoptotic effects on primary human acute myeloid leukaemia cells. Br. J. Haematol. 136, 814-828
21. Kisselev, A.F. and Goldberg, A.L. (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364-378
22. Lightcap, E.S., McCormack, T.A., Pien, C.S., Chau, V., Adams, J. and Elliott, P.J. (2000) Proteasome inhibition measurements: clinical application. Clin. Chem. 46, 673-683
23. Kisselev, A.F., Callard, A. and Goldberg, A.L. (2006) Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J. Biol. Chem. 281, 8582-8590
24. Luker, G.D., Pica, C.M., Song, J., Luker, K.E. and Piwnica-Worms, D. (2003) Imaging 26S proteasome activity and inhibition in living mice. Nat. Med. 9, 969-973
25. Dantuma, N.P., Lindsten, K., Glas, R., Jellne, M. and Masucci, M.G. (2000) Short-lived green fluorescent proteins for quantifying ubiquitin/ proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 18, 538-543
26. Lindsten, K., Menendez-Benito, V., Masucci, M.G. and Dantuma, N.P. (2003) A transgenic mouse model of the ubiquitin/proteasome system. Nat. Biotechnol. 21, 897-902
27. Berkers, C.R., van Leeuwen, F.W., Groothuis, T.A., Peperzak, V., van Tilburg, E.W., Borst, J., Neefjes, J.J. and Ovaa, H. (2007) Profiling proteasome activity in tissue with fluorescent probes. Mol. Pharm. 4, 739-748
28. Muchamuel, T., Basler, M., Aujay, M.A., Suzuki, E., Kalim, K.W., Lauer, C., Sylvain, C., Ring, E.R., Shields, J., Jiang, J. et al. (2009) A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat. Med. 15, 781-787
29. Parlati, F., Lee, S.J., Aujay, M., Suzuki, E., Levitsky, K., Lorens, J.B., Micklem, D.R., Ruurs, P., Sylvain, C., Lu, Y. et al. (2009) Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood 114, 3439-3447
30. Verdoes, M., Florea, B.I., Menendez-Benito, V., Maynard, C.J., Witte, M.D., van der Linden, W.A., van den Nieuwendijk, A.M., Hofmann, T., Berkers, C.R., van Leeuwen, F.W. et al. (2006) A fluorescent broad-spectrum proteasome inhibitor for labeling proteasomes in vitro and in vivo. Chem. Biol. 13, 1217-1226
31. Kraus, M., Ruckrich, T., Reich, M., Gogel, J., Beck, A., Kammer, W., Berkers, C.R., Burg, D., Overkleeft, H., Ovaa, H. and Driessen, C. (2007) Activity patterns of proteasome subunits reflect bortezomib sensitivity of hematologic malignancies and are variable in primary human leukemia cells. Leukemia 21, 84-92
32. Hoeller, D. and Dikic, I. (2009) Targeting the ubiquitin system in cancer therapy. Nature 458, 438-444
33. Chauhan, D., Singh, A., Brahmandam, M., Podar, K., Hideshima, T., Richardson, P., Munshi, N., Palladino, M.A. and Anderson, K.C. (2008) Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. Blood 111, 1654-1664
34. Lim, H.S., Archer, C.T. and Kodadek, T. (2007) Identification of a peptoid inhibitor of the proteasome 19S regulatory particle. J. Am. Chem. Soc. 129, 7750-7751
35. Lim, H.S., Cai, D., Archer, C.T. and Kodadek, T. (2007) Periodate-triggered cross-linking reveals Sug2/Rpt4 as the molecular target of a peptoid inhibitor of the 19S proteasome regulatory particle. J. Am. Chem. Soc. 129, 12936-12937
36. Soucy, T.A., Smith, P.G., Milhollen, M.A., Berger, A.J., Gavin, J.M., Adhikari, S., Brownell, J.E., Burke, K.E., Cardin, D.P., Critchley, S. et al. (2009) An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736
37. Roccaro, A.M., Leleu, X., Sacco, A., Jia, X., Melhem, M., Moreau, A.S., Ngo, H.T., Runnels, J., Azab, A., Azab, F. et al. (2008) Dual targeting of the proteasome regulates survival and homing in Waldenstrom macroglobulinemia. Blood 111, 4752-4763
38. kip1 in mediating antitumor activities in response to proteasome inhibition. Cancer Cell 14, 23-35
39. Nencioni, A., Grunebach, F., Patrone, F., Ballestrero, A. and Brossart, P. (2007) Proteasome inhibitors: antitumor effects and beyond. Leukemia 21, 30-36
40. Orlowski, R.Z., Voorhees, P.M., Garcia, R.A., Hall, M.D., Kudrik, F.J., Allred, T., Johri, A.R., Jones, P.E., Ivanova, A., Van Deventer, H.W. et al. (2005) Phase 1 trial of the proteasome inhibitor bortezomib and pegylated liposomal doxorubicin in patients with advanced hematologic malignancies. Blood 105, 3058-3065
41. Orlowski, R.Z., Nagler, A., Sonneveld, P., Blade, J., Hajek, R., Spencer, A., San Miguel, J., Robak, T., Dmoszynska, A., Horvath, N. et al. (2007) Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J. Clin. Oncol. 25, 3892-3901
42. Fenical, W., Jensen, P.R., Palladino, M.A., Lam, K.S., Lloyd, G.K. and Potts, B.C. (2009) Discovery and development of the anticancer agent salinosporamide A (NPI-0052). Bioorg. Med. Chem. 17, 2175-2180
43. Sanchez, E., Campbell, R., Steinberg, J., Li, M., Chen, H., Bonavida, B. and Berenson, J. (2008) The novel proteasome inhibitor CEP-18770 inhibits myeloma tumor growth in vitro and in vivo and enhances the anti-MM effects of melphalan, ASH Annual Meeting and Exposition, San Francisco, CA, U.S.A., 6-9 December 2008, Abstract 843
44. Egerer, T., Martinez-Gamboa, L., Dankof, A., Stuhlmuller, B., Dorner, T., Krenn, V., Egerer, K., Rudolph, P.E., Burmester, G.R. and Feist, E. (2006) Tissue-specific up-regulation of the proteasome subunit β5i (LMP7) in Sjogren's syndrome. Arthritis Rheum. 54, 1501-1508
45. Diaz-Hernandez, M., Hernandez, F., Martin-Aparicio, E., Gomez-Ramos, P., Moran, M.A., Castano, J.G., Ferrer, I., Avila, J. and Lucas, J.J. (2003) Neuronal induction of the immunoproteasome in Huntington's disease. J. Neurosci. 23, 11653-11661
46. Mishto, M., Bellavista, E., Santoro, A., Stolzing, A., Ligorio, C., Nacmias, B., Spazzafumo, L., Chiappelli, M., Licastro, F., Sorbi, S. et al. (2006) Immunoproteasome and LMP2 polymorphism in aged and Alzheimer's disease brains. Neurobiol. Aging 27, 54-66
47. Lin, G., Li, D., de Carvalho, L.P., Deng, H., Tao, H., Vogt, G., Wu, K., Schneider, J., Chidawanyika, T., Warren, J.D., Li, H. and Nathan, C. (2009) Inhibitors selective for mycobacterial versus human proteasomes. Nature 461, 621-626