Bafetinib (INNO-406) reverses multidrug resistance by inhibiting the efflux function of ABCB1 and ABCG2 transporters

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zhang, Yun Kai ^a   Zhang, Guan Nan ^a   Wang, Yi Jun ^a   Patel, Bhargav A ^a   Talele, Tanaji T ^a   Yang, Dong Hua ^a   Chen, Zhe Sheng ^a  

^a ST JOHN'S UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BAFETINIB; BREAST CANCER RESISTANCE PROTEIN; DOXORUBICIN; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; PYRIMIDINE DERIVATIVE; VANADIC ACID;

CHEMISTRY; DRUG EFFECTS; FLUORESCENCE; GENETICS; HUMAN; METABOLISM; MULTIDRUG RESISTANCE; MUTATION; PRECLINICAL STUDY; TIME FACTOR; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 2; ATP-BINDING CASSETTE, SUB-FAMILY B, MEMBER 1; CELL LINE, TUMOR; DOXORUBICIN; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, MULTIPLE; FLUORESCENCE; HUMANS; MITOXANTRONE; MUTATION; PACLITAXEL; PYRIMIDINES; TIME FACTORS; VANADATES;

EID: 84971201051     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep25694     Document Type: Article

References (42)

1. Wu, Q., Yang, Z., Nie, Y., Shi, Y. and Fan, D. Multi-drug resistance in cancer chemotherapeutics: mechanisms and lab approaches. Cancer Lett 347, 159-166, doi: 10.1016/j.canlet.2014.03.013 (2014).
2. Dean, M. and Annilo, T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6, 123-142, doi: 10.1146/annurev.genom.6.080604.162122 (2005).
3. Zhang, Y. K., Wang, Y. J., Gupta, P. and Chen, Z. S. Multidrug Resistance Proteins (MRPs) and Cancer Therapy. AAPS J 17, 802-812, doi: 10.1208/s12248-015-9757-1 (2015).
4. Borst, P. and Elferink, R. O. Mammalian ABC transporters in health and disease. Annu Rev Biochem 71, 537-592, doi: 10.1146/ annurev.biochem.71.102301.093055 (2002).
5. Fojo, T. and Coley, H. M. The role of efflux pumps in drug-resistant metastatic breast cancer: new insights and treatment strategies. Clin Breast Cancer 7, 749-756, doi: 10.3816/CBC.2007.n.035 (2007).
6. Han, J. Y. et al. Associations of ABCB1, ABCC2, and ABCG2 polymorphisms with irinotecan-pharmacokinetics and clinical outcome in patients with advanced non-small cell lung cancer. Cancer 110, 138-147, doi: 10.1002/cncr.22760 (2007).
7. Matsuo, K. et al. Multidrug resistance gene (MDR-1) and risk of brain metastasis in epithelial ovarian, fallopian tube, and peritoneal cancer. Am J Clin Oncol 34, 488-493, doi: 10.1097/COC.0b013e3181ec5f4b (2011).
8. Gao, B. et al. Paclitaxel sensitivity in relation to ABCB1 expression, efflux and single nucleotide polymorphisms in ovarian cancer. Sci Rep 4, 4669, doi: 10.1038/srep04669 (2014).
9. Sarkadi, B., Homolya, L., Szakacs, G. and Varadi, A. Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol Rev 86, 1179-1236, doi: 10.1152/physrev.00037.2005 (2006).
10. Wilson, C. S. et al. Gene expression profiling of adult acute myeloid leukemia identifies novel biologic clusters for risk classification and outcome prediction. Blood 108, 685-696, doi: 10.1182/blood-2004-12-4633 (2006).
11. Wang, Y. J., Zhang, Y. K., Kathawala, R. J. and Chen, Z. S. Repositioning of Tyrosine Kinase Inhibitors as Antagonists of ATP-Binding Cassette Transporters in Anticancer Drug Resistance. Cancers (Basel ) 6, 1925-1952, doi: 10.3390/cancers6041925 (2014).
12. Tiwari, A. K. et al. Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters. Biochem Pharmacol 78, 153-161, doi: 10.1016/j.bcp.2009.04.002 (2009).
13. Wang, D. S. et al. Icotinib antagonizes ABCG2-mediated multidrug resistance, but not the pemetrexed resistance mediated by thymidylate synthase and ABCG2. Oncotarget 5, 4529-4542, doi: 10.18632/oncotarget.2102 (2014).
14. Zhang, H. et al. In vitro, in vivo and ex vivo characterization of ibrutinib: a potent inhibitor of the efflux function of the transporter MRP1. Br J Pharmacol 171, 5845-5857, doi: 10.1111/bph.12889 (2014).
15. Nicolle, E. et al. Breast cancer resistance protein (BCRP/ABCG2): new inhibitors and QSAR studies by a 3D linear solvation energy approach. Eur J Pharm Sci 38, 39-46, doi: 10.1016/j.ejps.2009.05.012 (2009).
16. Chen, L., Li, Y., Yu, H., Zhang, L. and Hou, T. Computational models for predicting substrates or inhibitors of P-glycoprotein. Drug Discov Today 17, 343-351, doi: 10.1016/j.drudis.2011.11.003 (2012).
17. Ishikawa, T. et al. Quantitative structure-activity relationship (QSAR) analysis to predict drug-drug interactions of ABC transporter ABCG2. Mini Rev Med Chem 12, 505-514 (2012).
18. Aller, S. G. et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722, doi: 10.1126/science.1168750 (2009).
19. Li, J., Jaimes, K. F. and Aller, S. G. Refined structures of mouse P-glycoprotein. Protein Sci 23, 34-46, doi: 10.1002/pro.2387 (2014).
20. Robey, R. W. et al. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 89, 1971-1978, doi: 10.1038/sj.bjc.6601370 (2003).
21. Alqawi, O., Bates, S. and Georges, E. Arginine482 to threonine mutation in the breast cancer resistance protein ABCG2 inhibits rhodamine 123 transport while increasing binding. Biochem J 382, 711-716, doi: 10.1042/BJ20040355 (2004).
22. Klepsch, F., Vasanthanathan, P. and Ecker, G. F. Ligand and structure-based classification models for prediction of P-glycoprotein inhibitors. J Chem Inf Model 54, 218-229, doi: 10.1021/ci400289j (2014).
23. Santos, F. P., Kantarjian, H., Cortes, J. and Quintas-Cardama, A. Bafetinib, a dual Bcr-Abl/Lyn tyrosine kinase inhibitor for the potential treatment of leukemia. Curr Opin Investig Drugs 11, 1450-1465 (2010).
24. Portnow, J. et al. A neuropharmacokinetic assessment of bafetinib, a second generation dual BCR-Abl/Lyn tyrosine kinase inhibitor, in patients with recurrent high-grade gliomas. Eur J Cancer 49, 1634-1640, doi: 10.1016/j.ejca.2013.01.001 (2013).
25. Yokota, A. et al. INNO-406, a novel BCR-ABL/Lyn dual tyrosine kinase inhibitor, suppresses the growth of Ph+ leukemia cells in the central nervous system, and cyclosporine A augments its in vivo activity. Blood 109, 306-314, doi: 10.1182/blood-2006-03-013250 (2007).
26. Wang, Y. J. et al. Motesanib (AMG706), a potent multikinase inhibitor, antagonizes multidrug resistance by inhibiting the efflux activity of the ABCB1. Biochem Pharmacol 90, 367-378, doi: 10.1016/j.bcp.2014.06.006 (2014).
27. Anreddy, N. et al. Tyrosine kinase inhibitors as reversal agents for ABC transporter mediated drug resistance. Molecules 19, 13848-13877, doi: 10.3390/molecules190913848 (2014).
28. Shen, T. et al. Imatinib and nilotinib reverse multidrug resistance in cancer cells by inhibiting the efflux activity of the MRP7 (ABCC10). Plos One 4, e7520, doi: 10.1371/journal.pone.0007520 (2009).
29. Kathawala, R. J. et al. The small molecule tyrosine kinase inhibitor NVP-BHG712 antagonizes ABCC10-mediated paclitaxel resistance: a preclinical and pharmacokinetic study. Oncotarget 6, 510-521 (2015).
30. Castellino, S. M. et al. Flunarizine enhancement of melphalan activity against drug-sensitive/resistant rhabdomyosarcoma. Br J Cancer 71, 1181-1187 (1995).
31. Efferth, T. et al. Activity of drugs from traditional Chinese medicine toward sensitive and MDR1-or MRP1-overexpressing multidrug-resistant human CCRF-CEM leukemia cells. Blood Cells Mol Dis 28, 160-168 (2002).
32. Wang, Y. J. et al. Tea nanoparticle, a safe and biocompatible nanocarrier, greatly potentiates the anticancer activity of doxorubicin. Oncotarget, doi: 10.18632/oncotarget.6711 (2015).
33. Zhang, Y. K. et al. Semi-synthetic ocotillol analogues as selective ABCB1-mediated drug resistance reversal agents. Oncotarget 6, 24277-24290, doi: 10.18632/oncotarget.4493 (2015).
34. Galetti, M. et al. Effect of ABCG2/BCRP Expression on Efflux and Uptake of Gefitinib in NSCLC Cell Lines. Plos One 10, e0141795, doi: 10.1371/journal.pone.0141795 (2015).
35. Mao, Q. and Unadkat, J. D. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J 7, E118-133, doi: 10.1208/ aapsj070112 (2005).
36. Cutts, S. M., Swift, L. P., Rephaeli, A., Nudelman, A. and Phillips, D. R. Sequence specificity of adriamycin-DNA adducts in human tumor cells. Mol Cancer Ther 2, 661-670 (2003).
37. Shen, F. et al. Dynamic assessment of mitoxantrone resistance and modulation of multidrug resistance by valspodar (PSC833) in multidrug resistance human cancer cells. J Pharmacol Exp Ther 330, 423-429, doi: 10.1124/jpet.109.153551 (2009).
38. Germann, U. A. et al. Characterization of phosphorylation-defective mutants of human P-glycoprotein expressed in mammalian cells. J Biol Chem 271, 1708-1716 (1996).
39. Zhang, H. et al. WHI-P154 enhances the chemotherapeutic effect of anticancer agents in ABCG2-overexpressing cells. Cancer Sci 105, 1071-1078, doi: 10.1111/cas.12462 (2014).
40. Mares-Samano, S., Badhan, R. and Penny, J. Identification of putative steroid-binding sites in human ABCB1 and ABCG2. Eur J Med Chem 44, 3601-3611, doi: 10.1016/j.ejmech.2009.02.027 (2009).
41. Irwin, J. J., Sterling, T., Mysinger, M. M., Bolstad, E. S. and Coleman, R. G. ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52, 1757-1768, doi: 10.1021/ci3001277 (2012).
42. Huang, X. C. et al. Lamellarin O, a pyrrole alkaloid from an Australian marine sponge, Ianthella sp., reverses BCRP mediated drug resistance in cancer cells. Mar Drugs 12, 3818-3837, doi: 10.3390/md12073818 (2014).