Development of peptide-based reversing agents for P-glycoprotein-mediated resistance to carfilzomib

Molecular Pharmaceutics

Volumn 9, Issue 8, 2012, Pages 2197-2205

  Ao, Lin ^a   Wu, Ying ^a   Kim, Donghern ^a   Jang, Eun Ryoung ^a   Kim, Kyunghwa ^a   Lee, Do Min ^a   Kim, Kyung Bo ^a   Lee, Wooin ^a  

^a University of Kentucky   (United States)

Author keywords

acquired resistance; carfilzomib; P glycoprotein; resistance reversal; small peptides

Indexed keywords

BORTEZOMIB; CARFILZOMIB; GLYCOPROTEIN P; PACLITAXEL; PEPTIDE DERIVATIVE; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG; VERAPAMIL; YU 101;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG RESISTANCE; DRUG SENSITIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; STRUCTURE ANALYSIS; UPREGULATION;

BORONIC ACIDS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HUMANS; OLIGOPEPTIDES; P-GLYCOPROTEIN; PEPTIDES; PROTEASOME INHIBITORS; PYRAZINES; VERAPAMIL;

EID: 84864704046     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300044b     Document Type: Article

References (33)

1. Petroski, M. D. The ubiquitin system, disease, and drug discovery BMC Biochem. 2008, 9 (Suppl. 1) S7
2. Marques, A. J.; Palanimurugan, R.; Matias, A. C.; Ramos, P. C.; Dohmen, R. J. Catalytic mechanism and assembly of the proteasome Chem. Rev. 2009, 109, 1509-1536
3. Adams, J. The development of proteasome inhibitors as anticancer drugs Cancer Cell 2004, 5, 417-421 (Pubitemid 38610244)
4. Kuhn, D. J.; Orlowski, R. Z.; Bjorklund, C. C. Second Generation Proteasome Inhibitors: Carfilzomib and Immunoproteasome-Specific Inhibitors (IPSIs) Curr. Cancer Drug Targets 2011, 11, 285-295
5. Jain, S.; Diefenbach, C.; Zain, J.; O'Connor, O. A. Emerging role of carfilzomib in treatment of relapsed and refractory lymphoid neoplasms and multiple myeloma Core Evid. 2011, 6, 43-57
6. Arastu-Kapur, S.; Anderl, J. L.; Kraus, M.; Parlati, F.; Shenk, K. D.; Lee, S. J.; Muchamuel, T.; Bennett, M. K.; Driessen, C.; Ball, A. J.; Kirk, C. J. Non-proteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events Clin. Cancer Res. 2011, 17, 2734-2743
7. Adams, J.; Behnke, M.; Chen, S.; Cruickshank, A. A.; Dick, L. R.; Grenier, L.; Klunder, J. M.; Ma, Y. T.; Plamondon, L.; Stein, R. L. Potent and selective inhibitors of the proteasome: dipeptidyl boronic acids Bioorg. Med. Chem. Lett. 1998, 8, 333-338 (Pubitemid 28072702)
8. 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, 6383-6391 (Pubitemid 47037522)
9. Gutman, D.; Morales, A. A.; Boise, L. H. Acquisition of a multidrug-resistant phenotype with a proteasome inhibitor in multiple myeloma Leukemia 2009, 23, 2181-2183
10. Ivancsits, D.; Nimmanapali, R.; Sun, M.; Shenk, K.; Demo, S. D.; Bennett, M. K.; Dalton, W. S.; Alsina, M. The Proteasome Inhibitor PR-171 Inhibits Cell Growth, Induces Apoptosis, and Overcomes De Novo and Acquired Drug Resistance in Human Multiple Myeloma Cells Blood 2005, 106, 1575
11. Verbrugge, S. E.; Assaraf, Y. G.; Dijkmans, B. A.; Scheffer, G. L.; Al, M.; den Uyl, D.; Oerlemans, R.; Chan, E. T.; Kirk, C. J.; Peters, G. J.; van der Heijden, J. W.; de Gruijl, T. D.; Scheper, R. J.; Jansen, G. Inactivating PSMB5 mutations and P-glycoprotein (multidrug resistance-associated protein/ATP-binding cassette B1) mediate resistance to proteasome inhibitors: ex vivo efficacy of (immuno)proteasome inhibitors in mononuclear blood cells from patients with rheumatoid arthritis J. Pharmacol. Exp. Ther. 2012, 341, 174-182
12. Lu, S.; Yang, J.; Song, X.; Gong, S.; Zhou, H.; Guo, L.; Song, N.; Bao, X.; Chen, P.; Wang, J. Point mutation of the proteasome beta5 subunit gene is an important mechanism of bortezomib resistance in bortezomib-selected variants of Jurkat T cell lymphoblastic lymphoma/leukemia line J. Pharmacol. Exp. Ther. 2008, 326, 423-431
13. Fuchs, D.; Berges, C.; Opelz, G.; Daniel, V.; Naujokat, C. Increased expression and altered subunit composition of proteasomes induced by continuous proteasome inhibition establish apoptosis resistance and hyperproliferation of Burkitt lymphoma cells J. Cell. Biochem. 2008, 103, 270-283
14. Ri, M.; Iida, S.; Nakashima, T.; Miyazaki, H.; Mori, F.; Ito, A.; Inagaki, A.; Kusumoto, S.; Ishida, T.; Komatsu, H.; Shiotsu, Y.; Ueda, R. Bortezomib-resistant myeloma cell lines: a role for mutated PSMB5 in preventing the accumulation of unfolded proteins and fatal ER stress Leukemia 2010, 24, 1506-1512
15. Oerlemans, R.; Franke, N. E.; Assaraf, Y. G.; Cloos, J.; van Zantwijk, I.; Berkers, C. R.; Scheffer, G. L.; Debipersad, K.; Vojtekova, K.; Lemos, C.; van der Heijden, J. W.; Ylstra, B.; Peters, G. J.; Kaspers, G. L.; Dijkmans, B. A.; Scheper, R. J.; Jansen, G. Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein Blood 2008, 112, 2489-2499
16. Ruckrich, T.; Kraus, M.; Gogel, J.; Beck, A.; Ovaa, H.; Verdoes, M.; Overkleeft, H. S.; Kalbacher, H.; Driessen, C. Characterization of the ubiquitin-proteasome system in bortezomib-adapted cells Leukemia 2009, 23, 1098-1105
17. Zhang, L.; Littlejohn, J. E.; Cui, Y.; Cao, X.; Peddaboina, C.; Smythe, W. R. Characterization of bortezomib-adapted I-45 mesothelioma cells Mol. Cancer 2010, 9, 110
18. Gareau, C.; Fournier, M. J.; Filion, C.; Coudert, L.; Martel, D.; Labelle, Y.; Mazroui, R. p21 Upregulation through the Stress Granule-Associated Protein CUGBP1 Confers Resistance to Bortezomib-Mediated Apoptosis PLoS One 2011, 6, e20254
19. Elofsson, M.; Splittgerber, U.; Myung, J.; Mohan, R.; Crews, C. M. Towards subunit-specific proteasome inhibitors: synthesis and evaluation of peptide alpha,beta-epoxyketones Chem. Biol. 1999, 6, 811-822
20. Ho, Y. K.; Bargagna-Mohan, P.; Wehenkel, M.; Mohan, R.; Kim, K. B. LMP2-specific inhibitors: Chemical genetic tools for proteasome biology Chem. Biol. 2007, 14, 419-430 (Pubitemid 46617320)
21. Myung, J.; Kim, K. B.; Lindsten, K.; Dantuma, N. P.; Crews, C. M. Lack of proteasome active site allostery as revealed by subunit-specific inhibitors Mol. Cell 2001, 7, 411-420 (Pubitemid 32206508)
22. 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, 3028-3038
23. Sarkadi, B.; Muller, M.; Homolya, L.; Hollo, Z.; Seprodi, J.; Germann, U. A.; Gottesman, M. M.; Price, E. M.; Boucher, R. C. Interaction of bioactive hydrophobic peptides with the human multidrug transporter FASEB J. 1994, 8, 766-770 (Pubitemid 24229772)
24. Sharom, F. J.; Lu, P.; Liu, R.; Yu, X. Linear and cyclic peptides as substrates and modulators of P-glycoprotein: peptide binding and effects on drug transport and accumulation Biochem. J. 1998, 333 (Part 3) 621-630 (Pubitemid 28398529)
25. Sharom, F. J.; DiDiodato, G.; Yu, X.; Ashbourne, K. J. Interaction of the P-glycoprotein multidrug transporter with peptides and ionophores J. Biol. Chem. 1995, 270, 10334-10341
26. Sharom, F. J.; Yu, X.; Lu, P.; Liu, R.; Chu, J. W.; Szabo, K.; Muller, M.; Hose, C. D.; Monks, A.; Varadi, A.; Seprodi, J.; Sarkadi, B. Interaction of the P-glycoprotein multidrug transporter (MDR1) with high affinity peptide chemosensitizers in isolated membranes, reconstituted systems, and intact cells Biochem. Pharmacol. 1999, 58, 571-586 (Pubitemid 29296877)
27. Yang, J.; Wang, Z.; Fang, Y.; Jiang, J.; Zhao, F.; Wong, H.; Bennett, M. K.; Molineaux, C. J.; Kirk, C. J. Pharmacokinetics, pharmacodynamics, metabolism, distribution, and excretion of carfilzomib in rats Drug Metab. Dispos. 2011, 39, 1873-1882
28. Minderman, H.; Zhou, Y.; O'Loughlin, K. L.; Baer, M. R. Bortezomib activity and in vitro interactions with anthracyclines and cytarabine in acute myeloid leukemia cells are independent of multidrug resistance mechanisms and p53 status Cancer Chemother. Pharmacol. 2007, 60, 245-255 (Pubitemid 46742540)
29. de Wilt, L. H.; Jansen, G.; Assaraf, Y. G.; van Meerloo, J.; Cloos, J.; Schimmer, A. D.; Chan, E. T.; Kirk, C. J.; Peters, G. J.; Kruyt, F. A. Proteasome-based mechanisms of intrinsic and acquired bortezomib resistance in non-small cell lung cancer Biochem. Pharmacol. 2012, 83, 207-217
30. Gutmann, D. A.; Ward, A.; Urbatsch, I. L.; Chang, G.; van Veen, H. W. Understanding polyspecificity of multidrug ABC transporters: Closing in on the gaps in ABCB1 Trends Biochem. Sci. 2010, 35, 36-42
31. Aller, S. G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P. M.; Trinh, Y. T.; Zhang, Q.; Urbatsch, I. L.; Chang, G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 2009, 323, 1718-1722
32. Klepsch, F.; Jabeen, I.; Chiba, P.; Ecker, G. F. Pharmacoinformatic approaches to design natural product type ligands of ABC-transporters Curr. Pharm. Des. 2010, 16, 1742-1752
33. Bikadi, Z.; Hazai, I.; Malik, D.; Jemnitz, K.; Veres, Z.; Hari, P.; Ni, Z.; Loo, T. W.; Clarke, D. M.; Hazai, E.; Mao, Q. Predicting P-Glycoprotein-Mediated Drug Transport Based On Support Vector Machine and Three-Dimensional Crystal Structure of P-glycoprotein PLoS One 2011, 6, e25815