Telatinib reverses chemotherapeutic multidrug resistance mediated by ABCG2 efflux transporter in vitro and in vivo

Biochemical Pharmacology

Volumn 89, Issue 1, 2014, Pages 52-61

  Sodani, Kamlesh ^a   Patel, Atish ^a   Anreddy, Nagaraju ^a   Singh, Satyakam ^a   Yang, Dong Hua ^b   Kathawala, Rishil J ^a   Kumar, Priyank ^a   Talele, Tanaji T ^a   Chen, Zhe Sheng ^a  

^a ST JOHN'S UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

ABC transporter; ABCG2; Multidrug resistance; Telatinib; Tyrosine kinase inhibitor

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BREAST CANCER RESISTANCE PROTEIN; DOXORUBICIN; MITOXANTRONE; TELATINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; TUMOR VOLUME; XENOGRAFT;

ABC TRANSPORTER; ABCG2; MULTIDRUG RESISTANCE; TELATINIB; TYROSINE KINASE INHIBITOR;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, NEOPLASM; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM PROTEINS; PYRIDAZINES; PYRIDINES;

EID: 84897994292     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.02.012     Document Type: Article

References (52)

1. M.M. Gottesman Mechanisms of cancer drug resistance Annu Rev Med 53 2002 615 627 (Pubitemid 34177898)
2. R.G. Deeley, C. Westlake, and S.P. Cole Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins Physiol Rev 86 2006 849 899 (Pubitemid 44033384)
3. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat Rev Cancer 2 2002 48 58 (Pubitemid 37328807)
4. M. Dean The human ATP-binding cassette (ABC) transporter superfamily Genome Res 11 2001 1156 1166 (Pubitemid 32677289)
5. M.M. Gottesman, and S.V. Ambudkar Overview ABC transporters and human disease J Bioenerg Biomembr 33 2001 453 458 (Pubitemid 34052570)
6. J.P. Gillet, T. Efferth, and J. Remacle Chemotherapy-induced resistance by ATP-binding cassette transporter genes Biochim Biophys Acta 1775 2007 237 262 (Pubitemid 46899341)
7. W. Loscher, and H. Potschka Drug resistance in brain diseases and the role of drug efflux transporters Nat Rev Neurosci 6 2005 591 602 (Pubitemid 41059334)
8. G. Szakacs, A. Varadi, C. Ozvegy-Laczka, and B. Sarkadi The role of ABC transporters in drug absorption, distribution, metabolism, excretion and toxicity (ADME-Tox) Drug Discov Today 13 2008 379 393
9. R.W. Robey, O. Polgar, J. Deeken, K.W. To, and S.E. Bates ABCG2: determining its relevance in clinical drug resistance Cancer Metastasis Rev 26 2007 39 57 (Pubitemid 46452182)
10. A.K. Tiwari, K. Sodani, C.L. Dai, C.R. Ashby Jr., and Z.S. Chen Revisiting the ABCs of multidrug resistance in cancer chemotherapy Curr Pharm Biotechnol 12 2011 570 594
11. R.W. Robey, C. Ierano, Z. Zhan, and S.E. Bates The challenge of exploiting ABCG2 in the clinic Curr Pharm Biotechnol 12 2011 595 608
12. K. Natarajan, Y. Xie, M.R. Baer, and D.D. Ross Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance Biochem Pharmacol 83 2012 1084 1103
13. D. Steinbach, W. Sell, A. Voigt, J. Hermann, F. Zintl, and A. Sauerbrey BCRP gene expression is associated with a poor response to remission induction therapy in childhood acute myeloid leukemia Leukemia 16 2002 1443 1447
14. M.M. van den Heuvel-Eibrink, E.A. Wiemer, A. Prins, J.P. Meijerink, P.J. Vossebeld, and B. van der Holt et al. Increased expression of the breast cancer resistance protein (BCRP) in relapsed or refractory acute myeloid leukemia (AML) Leukemia 16 2002 833 839 (Pubitemid 34537555)
15. L. Candeil, I. Gourdier, D. Peyron, N. Vezzio, V. Copois, and F. Bibeau et al. ABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan-treated metastases Int J Cancer 109 2004 848 854 (Pubitemid 38500741)
16. J.E. Diestra, G.L. Scheffer, I. Catala, M. Maliepaard, J.H. Schellens, and R.J. Scheper et al. Frequent expression of the multi-drug resistance-associated protein BCRP/MXR/ABCP/ABCG2 in human tumours detected by the BXP-21 monoclonal antibody in paraffin-embedded material J Pathol 198 2002 213 219 (Pubitemid 35243879)
17. S. Galimberti, F. Guerrini, G.A. Palumbo, U. Consoli, R. Fazzi, and F. Morabito et al. Evaluation of BCRP and MDR-1 co-expression by quantitative molecular assessment in AML patients Leuk Res 28 2004 367 372 (Pubitemid 38199944)
18. S. Zhou, J.D. Schuetz, K.D. Bunting, A.M. Colapietro, J. Sampath, and J.J. Morris et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype Nat Med 7 2001 1028 1034 (Pubitemid 32937383)
19. B.L. Abbott ABCG2 (BCRP) expression in normal and malignant hematopoietic cells Hematol Oncol 21 2003 115 130 (Pubitemid 37305331)
20. C. Hirschmann-Jax, A.E. Foster, G.G. Wulf, J.G. Nuchtern, T.W. Jax, and U. Gobel et al. A distinct "side population" of cells with high drug efflux capacity in human tumor cells Proc Natl Acad Sci U S A 101 2004 14228 14233 (Pubitemid 39305058)
21. J.E. Visvader, and G.J. Lindeman Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nat Rev Cancer 8 2008 755 768
22. A.M. Bleau, D. Hambardzumyan, T. Ozawa, E.I. Fomchenko, J.T. Huse, and C.W. Brennan et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells Cell Stem Cell 4 2009 226 235
23. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111 (Pubitemid 33041634)
24. M. Dean, T. Fojo, and S. Bates Tumour stem cells and drug resistance Nat Rev Cancer 5 2005 275 284 (Pubitemid 40488633)
25. S.K. Rabindran, H. He, M. Singh, E. Brown, K.I. Collins, and T. Annable et al. Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C Cancer Res 58 1998 5850 5858 (Pubitemid 29006428)
26. C.L. Dai, A.K. Tiwari, C.P. Wu, Su Xd, S.R. Wang, and Liu Dg et al. Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2 Cancer Res 68 2008 7905 7914
27. Z. Shi, X.X. Peng, I.W. Kim, S. Shukla, Q.S. Si, and R.W. Robey et al. Erlotinib (Tarceva, OSI-774) antagonizes ATP-binding cassette subfamily B member 1 and ATP-binding cassette subfamily G member 2 mediated drug resistance Cancer Res 67 2007 11012 11020 (Pubitemid 350145931)
28. K. Sodani, A.K. Tiwari, S. Singh, A. Patel, Z.J. Xiao, and J.J. Chen et al. GW583340 and GW2974, human EGFR and HER-2 inhibitors, reverse ABCG2- and ABCB1-mediated drug resistance Biochem Pharmacol 83 2012 1613 1622
29. A.K. Tiwari, K. Sodani, S.R. Wang, Y.H. Kuang, C.R. Ashby Jr., and X. Chen et al. Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters Biochem Pharmacol 78 2009 153 161
30. A.K. Tiwari, K. Sodani, C.L. Dai, A.H. Abuznait, S. Singh, and Z.J. Xiao et al. Nilotinib potentiates anticancer drug sensitivity in murine ABCB1-, ABCG2-, and ABCC10-multidrug resistance xenograft models Cancer Lett 328 2013 307 317
31. F.A. Eskens, N. Steeghs, J. Verweij, J.L. Bloem, O. Christensen, and L. van Doorn et al. Phase I dose escalation study of telatinib, a tyrosine kinase inhibitor of vascular endothelial growth factor receptor 2 and 3, platelet-derived growth factor receptor beta, and c-Kit, in patients with advanced or metastatic solid tumors J Clin Oncol 27 2009 4169 4176
32. K. Sodani, A. Patel, R.J. Kathawala, and Z.S. Chen Multidrug resistance associated proteins in multidrug resistance Chin J Cancer 31 2012 58 72
33. C.I. Bliss The calculation of the dosage-mortality curve Ann Appl Biol 22 1935 134 167
34. B. Sarkadi, E.M. Price, R.C. Boucher, U.A. Germann, and G.A. Scarborough Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase J Biol Chem 267 1992 4854 4858
35. Z.S. Chen, R.W. Robey, M.G. Belinsky, I. Shchaveleva, X.Q. Ren, and Y. Sugimoto et al. Transport of methotrexate, methotrexate polyglutamates, and 17beta-estradiol 17-(beta-d-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport Cancer Res 63 2003 4048 4054 (Pubitemid 36917926)
36. S.G. Aller, J. Yu, A. Ward, Y. Weng, S. Chittaboina, and R. Zhuo et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323 2009 1718 1722
37. M.F. Rosenberg, Z. Bikadi, J. Chan, X. Liu, Z. Ni, and X. Cai et al. The human breast cancer resistance protein (BCRP/ABCG2) shows conformational changes with mitoxantrone Structure 18 2010 482 493
38. E. Hazai, and Z. Bikadi Homology modeling of breast cancer resistance protein (ABCG2) J Struct Biol 162 2008 63 74
39. R.W. Robey, Y. Honjo, K. Morisaki, T.A. Nadjem, S. Runge, and M. Risbood et al. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity Br J Cancer 89 2003 1971 1978 (Pubitemid 37533279)
40. H. Mitomo, R. Kato, A. Ito, S. Kasamatsu, Y. Ikegami, and I. Kii et al. A functional study on polymorphism of the ATP-binding cassette transporter ABCG2: critical role of arginine-482 in methotrexate transport Biochem J 373 2003 767 774 (Pubitemid 36981086)
41. M. Miwa, S. Tsukahara, E. Ishikawa, S. Asada, Y. Imai, and Y. Sugimoto Single amino acid substitutions in the transmembrane domains of breast cancer resistance protein (BCRP) alter cross resistance patterns in transfectants Int J Cancer 107 2003 757 763 (Pubitemid 37339729)
42. O. Alqawi, S. Bates, and E. Georges Arginine482 to threonine mutation in the breast cancer resistance protein ABCG2 inhibits rhodamine 123 transport while increasing binding Biochem J 382 2004 711 716 (Pubitemid 39243937)
43. C. Hegedus, K. Truta-Feles, G. Antalffy, G. Varady, K. Nemet, and C. Ozvegy-Laczka et al. Interaction of the EGFR inhibitors gefitinib, vandetanib, pelitinib and neratinib with the ABCG2 multidrug transporter: implications for the emergence and reversal of cancer drug resistance Biochem Pharmacol 84 2012 260 267
44. C. Hegedus, C. Özvegy-Laczka, Á. Apáti, M. Magócsi, K. Német, and L. Orfi et al. Interaction of nilotinib, dasatinib and bosutinib with ABCB1 and ABCG2: implications for altered anti-cancer effects and pharmacological properties Br J Pharmacol 158 2009 1153 1164
45. R. Yamazaki, Y. Nishiyama, T. Furuta, H. Hatano, Y. Igarashi, and N. Asakawa et al. Novel acrylonitrile derivatives, YHO-13177 and YHO-13351, reverse BCRP/ABCG2-mediated drug resistance in vitro and in vivo Mol Cancer Ther 10 2011 1252 1263
46. V. Goler-Baron, I. Sladkevich, and Y.G. Assaraf Inhibition of the PI3K-Akt signaling pathway disrupts ABCG2-rich extracellular vesicles and overcomes multidrug resistance in breast cancer cells Biochem Pharmacol 83 2012 1340 1348
47. K. Natarajan, J. Bhullar, S. Shukla, M. Burcu, Z.S. Chen, and S.V. Ambudkar et al. The Pim kinase inhibitor SGI-1776 decreases cell surface expression of P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and drug transport by Pim-1-dependent and -independent mechanisms Biochem Pharmacol 85 2013 514 524
48. K.K. To, and B. Tomlinson Targeting the ABCG2-overexpressing multidrug resistant (MDR) cancer cells by PPARgamma agonists Br J Pharmacol 170 2013 1137 1151
49. A. Brozik, C. Hegedus, Z. Erdei, T. Hegedus, C. Ozvegy-Laczka, and G. Szakacs et al. Tyrosine kinase inhibitors as modulators of ATP binding cassette multidrug transporters: substrates, chemosensitizers or inducers of acquired multidrug resistance Expert Opin Drug Metab Toxicol 7 2011 623 642
50. G. Ecker, and P. Chiba Transporters as drug carriers: structure, function, substrates 2009 Wiley-VCH Weinheim
51. D. Strumberg, B. Schultheis, I.A. Adamietz, O. Christensen, M. Buechert, and J. Kraetzschmar et al. Phase I dose escalation study of telatinib (BAY 57-9352) in patients with advanced solid tumours Br J Cancer 99 2008 1579 1585
52. K. Mross, A. Frost, M.E. Scheulen, J. Krauss, D. Strumberg, and B. Schultheiss et al. Phase I study of telatinib (BAY 57-9352): analysis of safety, pharmacokinetics, tumor efficacy and biomarkers in patients with colorectal cancer Vasc Cell 3 2011 16