Incorporation of non-natural amino acids improves cell permeability and potency of specific inhibitors of proteasome trypsin-like sites

Journal of Medicinal Chemistry

Volumn 56, Issue 3, 2013, Pages 1262-1275

  Geurink, Paul P ^a,e   Van Der Linden, Wouter A ^a,f   Mirabella, Anne C ^b,g   Gallastegui, Nerea ^c   De Bruin, Gerjan ^a   Blom, Annet E M ^a   Voges, Mathias J ^a   Mock, Elliot D ^a   Florea, Bogdan I ^a   Van Der Marel, Gijs A ^a   Driessen, Christoph ^d   Van Der Stelt, Mario ^a   Groll, Michael ^c   Overkleeft, Herman S ^a   Kisselev, Alexei F ^b  

^a NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c Munich Center for Integrated Protein Science   (Germany)

^d Kantonsspital St Gallen ^*  (Switzerland)

^e NETHERLANDS CANCER INSTITUTE   (Netherlands)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 [[(BENZYLOXY)CARBONYL]AMINO] 3 [4 [(2,2,2 TRICHLOROACETAMIDO)METHYL]PHENYL]PROPANOIC ACID; 2 [[(BENZYLOXY)CARBONYL]AMINO] 3 [4 [[(TERT BUTOXYCARBONYL)AMINO]METHYL]PHENYL] N METHOXY N METHYLPROPIONAMIDE; 2 [[(BENZYLOXY)CARBONYL]AMINO] 3 [4 [[(TERTBUTOXYCARBONYL)METHYL]PHENYL]PROPANOIC ACID; ANTINEOPLASTIC AGENT; AZIDO PHENYLLEUCINYLLEUCINYL 4 AMINOMETHYLPHENYLMETHYLVINYL SULFONE; BORTEZOMIB; CARFILZOMIB; DOXORUBICIN; PROTEASOME INHIBITOR; TERT BUTYL 4 [3 [METHOXY(METHYL)AMINO] 3 OXO 2 (TRITYLAMINO)PROPYL]BENZYLCARBAMATE; TRYPTASE INHIBITOR; UNCLASSIFIED DRUG; VORINOSTAT;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; DRUG POTENTIATION; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; HUMAN CELL; HYDROGEN BOND; MYELOMA CELL; NONHUMAN;

AMINO ACIDS; CELL LINE; CELL MEMBRANE PERMEABILITY; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; PROTEASOME INHIBITORS; TRYPSIN;

EID: 84873924284     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm3016987     Document Type: Article

References (43)

1. 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.; Shenk, K. D.; Smyth, M. S.; Sun, C. M.; Vallone, M. K.; Woo, T. M.; Molineaux, C. J.; Bennett, M. K. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome Cancer Res. 2007, 67 (13) 6383-6391
2. O'Connor, O. A.; Stewart, A. K.; Vallone, M.; Molineaux, C. J.; Kunkel, L. A.; Gerecitano, J. F.; Orlowski, R. Z. A phase 1 dose escalation study of the safety and pharmacokinetics of the novel proteasome inhibitor carfilzomib (PR-171) in patients with hematologic malignancies Clin. Cancer Res. 2009, 15 (22) 7085-7091
3. Chauhan, D.; Catley, L.; Li, G.; Podar, K.; Hideshima, T.; Velankar, M.; Mitsiades, C.; Mitsiades, N.; Yasui, H.; Letai, A.; Ovaa, H.; Berkers, C.; Nicholson, B.; Chao, T. H.; Neuteboom, S. T.; Richardson, P.; Palladino, M. A.; Anderson, K. C. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib Cancer Cell 2005, 8 (5) 407-419
4. Piva, R.; Ruggeri, B.; Williams, M.; Costa, G.; Tamagno, I.; Ferrero, D.; Giai, V.; Coscia, M.; Peola, S.; Massaia, M.; Pezzoni, G.; Allievi, C.; Pescalli, N.; Cassin, M.; di Giovine, S.; Nicoli, P.; de Feudis, P.; Strepponi, I.; Roato, I.; Ferracini, R.; Bussolati, B.; Camussi, G.; Jones-Bolin, S.; Hunter, K.; Zhao, H.; Neri, A.; Palumbo, A.; Berkers, C.; Ovaa, H.; Bernareggi, A.; Inghirami, G. CEP-18770: A novel, orally active proteasome inhibitor with a tumor-selective pharmacologic profile competitive with bortezomib Blood 2008, 111 (5) 2765-2775
5. Kupperman, E.; Lee, E. C.; Cao, Y.; Bannerman, B.; Fitzgerald, M.; Berger, A.; Yu, J.; Yang, Y.; Bruzzese, F.; Liu, J.; Blank, J.; Garcia, K.; Tsu, C.; Dick, L.; Fleming, P.; Yu, L.; Manfredi, M.; Rolfe, M.; Bolen, J. Evaluation of the proteasome inhibitor MLN9708 in preclinical models of human cancer Cancer Res. 2010, 70 (5) 1970-1980
6. Zhou, H. J.; Aujay, M. A.; Bennett, M. K.; Dajee, M.; Demo, S. D.; Fang, Y.; Ho, M. N.; Jiang, J.; Kirk, C. J.; Laidig, G. J.; Lewis, E. R.; Lu, Y.; Muchamuel, T.; Parlati, F.; Ring, E.; Shenk, K. D.; Shields, J.; Shwonek, P. J.; Stanton, T.; Sun, C. M.; Sylvain, C.; Woo, T. M.; Yang, J. Design and synthesis of an orally bioavailable and selective peptide epoxyketone proteasome inhibitor (PR-047) J. Med. Chem. 2009, 52 (9) 3028-3038
7. Adams, J. The development of proteasome inhibitors as anticancer drugs Cancer Cell 2004, 5 (5) 417-421
8. Kisselev, A. F.; Callard, A.; Goldberg, A. L. Importance of different active sites in protein breakdown by 26S proteasomes and the efficacy of proteasome inhibitors varies with the protein substrate J. Biol. Chem. 2006, 281 (13) 8583-8590
9. Altun, M.; Galardy, P. J.; Shringarpure, R.; Hideshima, T.; LeBlanc, R.; Anderson, K. C.; Ploegh, H. L.; Kessler, B. M. Effects of PS-341 on the activity and composition of proteasomes in multiple myeloma cells Cancer Res. 2005, 65 (17) 7896-7901
10. Berkers, C. R.; Verdoes, M.; Lichtman, E.; Fiebiger, E.; Kessler, B. M.; Anderson, K. C.; Ploegh, H. L.; Ovaa, H.; Galardy, P. J. Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib Nat. Methods 2005, 2 (5) 357-362
11. Britton, M.; Lucas, M. M.; Downey, S. L.; Screen, M.; Pletnev, A. A.; Verdoes, M.; Tokhunts, R. A.; Amir, O.; Goddard, A. L.; Pelphrey, P. M.; Wright, D. L.; Overkleeft, H. S.; Kisselev, A. F. Selective inhibitor of proteasome's caspase-like sites sensitizes cells to specific inhibition of chymotrypsin-like sites Chem. Biol. 2009, 16 (12) 1278-1289
12. Mirabella, A. C.; Pletnev, A. A.; Downey, S. L.; Florea, B. I.; Shabaneh, T. B.; Britton, M.; Verdoes, M.; Filippov, D. V.; Overkleeft, H. S.; Kisselev, A. F. Specific cell-permeable inhibitor of proteasome trypsin-like sites selectively sensitizes myeloma cells to bortezomib and carfilzomib Chem. Biol. 2011, 18 (5) 608-618
13. Screen, M.; Britton, M.; Downey, S. L.; Verdoes, M.; Voges, M. J.; Blom, A. E.; Geurink, P. P.; Risseeuw, M. D.; Florea, B. I.; van der Linden, W. A.; Pletnev, A. A.; Overkleeft, H. S.; Kisselev, A. F. Nature of pharmacophore influences active site specificity of proteasome inhibitors J. Biol. Chem. 2010, 285 (51) 40125-40134
14. Verdoes, M.; Willems, L. I.; van der Linden, W. A.; Duivenvoorden, B. A.; van der Marel, G. A.; Florea, B. I.; Kisselev, A. F.; Overkleeft, H. S. A panel of subunit-selective activity-based proteasome probes Org. Biomol. Chem 2010, 8 (12) 2719-2727
15. Groll, M.; Nazif, T.; Huber, R.; Bogyo, M. Probing structural determinants distal to the site of hydrolysis that control substrate specificity of the 20S proteasome Chem. Biol. 2002, 9 (5) 655-662
16. Köhler, A.; Cascio, P.; Leggett, D. S.; Woo, K. M.; Goldberg, A. L.; Finley, D. The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release Mol. Cell 2001, 7 (6) 1143-1152
17. Huber, E. M.; Basler, M.; Schwab, R.; Heinemeyer, W.; Kirk, C. J.; Groettrup, M.; Groll, M. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity Cell 2012, 148 (4) 727-738
18. Unno, M.; Mizushima, T.; Morimoto, Y.; Tomisugi, Y.; Tanaka, K.; Yasuoka, N.; Tsukihara, T. The structure of the mammalian 20S proteasome at 2.75 A resolution Structure 2002, 10 (5) 609-618
19. Kirschke, H.; Wiederanders, B. Cathepsin S and related lysosomal endopeptidases Methods Enzymol. 1994, 244, 500-511
20. Mitsiades, N.; Mitsiades, C. S.; Richardson, P. G.; Poulaki, V.; Tai, Y. T.; Chauhan, D.; Fanourakis, G.; Gu, X.; Bailey, C.; Joseph, M.; Libermann, T. A.; Schlossman, R.; Munshi, N. C.; Hideshima, T.; Anderson, K. C. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications Blood 2003, 101 (6) 2377-2380
21. Hideshima, T.; Richardson, P.; Chauhan, D.; Palombella, V. J.; Elliot, P. J.; Adams, J.; Anderson, K. C. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells Cancer Res. 2001, 61, 3071-3076
22. Geurink, P. P.; Liu, N.; Spaans, M. P.; Downey, S. L.; van den Nieuwendijk, A. M.; van der Marel, G. A.; Kisselev, A. F.; Florea, B. I.; Overkleeft, H. S. Incorporation of fluorinated phenylalanine generates highly specific inhibitor of proteasome's chymotrypsin-like sites J. Med. Chem. 2010, 53 (5) 2319-2323
23. Nazif, T.; Bogyo, M. Global analysis of proteasomal substrate specificity using positional-scanning libraries of covalent inhibitors Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (6) 2967-2972
24. Mohamed, M. M.; Sloane, B. F. Cysteine cathepsins: multifunctional enzymes in cancer Nat. Rev. Cancer 2006, 6 (10) 764-775
25. Rivier, J. E.; Jiang, G.; Porter, J.; Hoeger, C. A.; Craig, A. G.; Corrigan, A.; Vale, W.; Rivier, C. L. Gonadotropin-releasing hormone antagonists: novel members of the azaline B family J. Med. Chem. 1995, 38 (14) 2649-2662
26. Stokker, G.; Hoffman, W.; Homnick, C. A simple and inexpensive synthesis of 4-(aminomethyl)- l -phenylalanine J. Org. Chem. 1993, 58, 5015-5016
27. Verdoes, M.; Hillaert, U.; Florea, B. I.; Sae-Heng, M.; Risseeuw, M. D.; Filippov, D. V.; van der Marel, G. A.; Overkleeft, H. S. Acetylene functionalized BODIPY dyes and their application in the synthesis of activity based proteasome probes Bioorg. Med. Chem. Lett. 2007, 17 (22) 6169-6171
28. Verdoes, M.; Florea, B. I.; Menendez-Benito, V.; Witte, M. D.; van der Linden, W. A.; van den Nieuwendijk, A. M. C. H.; Hofmann, T.; Berkers, C.; van Leeuwen, F. W. B.; Groothuis, T. A.; Leeuwenburgh, M. A.; Ovaa, H.; Neefjes, J.; Filippov, D. V.; van der Marel, G. A.; Dantuma, N. P.; Overkleeft, H. S. A fluorescent broad spectrum proteasome inhibitor for labeling proteasomes in vitro and in vivo Chem. Biol. 2006, 13 (11) 1217-1226
29. Florea, B. I.; Verdoes, M.; Li, N.; van der Linden, W. A.; Geurink, P. P.; van den Elst, H.; Hofmann, T.; de Ru, A.; van Veelen, P. A.; Tanaka, K.; Sasaki, K.; Murata, S.; den Dulk, H.; Brouwer, J.; Ossendorp, F. A.; Kisselev, A. F.; Overkleeft, H. S. Activity-based profiling reveals reactivity of the murine thymoproteasome-specific subunit beta5t Chem. Biol. 2010, 17 (8) 795-801
30. Groll, M.; Ditzel, L.; Löwe, J.; Stock, D.; Bochtler, M.; Bartunik, H.; Huber, R. Structure of 20S proteasome from yeast at 2.4 Å resolution Nature 1997, 386 (6624) 463-471
31. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 1993, 26, 795-800
32. Brunger, A. T.; Adams, P. D.; Clore, G. M.; DeLano, W. L.; Gros, P.; Grosse-Kunstleve, R. W.; Jiang, J. S.; Kuszewski, J.; Nilges, M.; Pannu, N. S.; Read, R. J.; Rice, L. M.; Simonson, T.; Warren, G. L. Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 1998, 54 (Pt 5) 905-921
33. Brunger, A. T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures Nature 1992, 355 (6359) 472-475
34. Turk, D. Improvement of a programm for molecular graphics and manipulation of electron densities and its application for protein structure determination. Technical University, Munich, 1992.
35. Homer, R. W.; Swanson, J.; Jilek, R. J.; Hurst, T.; Clark, R. D. SYBYL line notation (SLN): a single notation to represent chemical structures, queries, reactions, and virtual libraries J. Chem. Inf. Model. 2008, 48 (12) 2294-2307
36. Ihlenfeldt, W. D.; Bolton, E. E.; Bryant, S. H. The PubChem chemical structure sketcher J. Cheminf. 2009, 1 (1) 20
37. Emsley, P.; Lohkamp, B.; Scott, W. G.; Cowtan, K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66 (Pt 4) 486-501
38. Vagin, A. A.; Steiner, R. A.; Lebedev, A. A.; Potterton, L.; McNicholas, S.; Long, F.; Murshudov, G. N. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60 (Pt 12, #1) 2184-2195
39. Vaguine, A. A.; Richelle, J.; Wodak, S. J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55 (Pt 1) 191-205
40. Kraulis, P. J. MOLSCRIPT: A Program to Produce Both Detailed and Schematic Plots of Protein Structures, 1991.
41. Esnouf, R. M. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities J. Mol. Graph. Model. 1997, 15 (2) 132-134 112-133.
42. DeLano, W. L. Unraveling hot spots in binding interfaces: progress and challenges Curr. Opin. Struct. Biol. 2002, 12 (1) 14-20
43. Löwe, J.; Stock, D.; Jap, B.; Zwickl, P.; Baumeister, W.; Huber, R. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution Science 1995, 268 (5210) 533-539