Repositioning of tyrosine kinase inhibitors as antagonists of ATP-binding cassette transporters in anticancer drug resistance

Cancers

Volumn 6, Issue 4, 2014, Pages 1925-1952

  Wang, Yi Jun ^a   Zhang, Yun Kai ^a   Kathawala, Rishil J ^a   Chen, Zhe Sheng ^a  

^a ST JOHN'S UNIVERSITY   (United States)

Author keywords

ABC transporters; Clinical relevance; Multidrug resistance; Pharmacogenomics; Tyrosine kinase inhibitor

Indexed keywords

ABC TRANSPORTER; AST 1306; BREAST CANCER RESISTANCE PROTEIN; GEFITINIB; IRINOTECAN; LAPATINIB; LINSITINIB; MASITINIB; METHOTREXATE; MITOXANTRONE; MOTESANIB; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 10; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; MULTIDRUG RESISTANCE PROTEIN 7; NILOTINIB; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; ROMIDEPSIN; TELATINIB; TENOFOVIR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALSPODAR; VEMURAFENIB; WHI P 154; ZOSUQUIDAR;

ABCB1 GENE; ABCC1 GENE; ABCC10 GENE; ABCC2 GENE; ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SURVIVAL; CELLULAR DISTRIBUTION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG TARGETING; DRUG TREATMENT FAILURE; GENETIC VARIABILITY; HUMAN; HYDROPHOBICITY; MOLECULAR WEIGHT; MULTIDRUG RESISTANCE; NONHUMAN; OVERALL SURVIVAL; PHARMACOGENOMICS; PROGRESSION FREE SURVIVAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR GENE; TUMOR REGRESSION; TUMOR VOLUME;

EID: 84907672366     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers6041925     Document Type: Review

References (159)

1. Cockerill, G.S.; Lackey, K.E. Small molecule inhibitors of the class 1 receptor tyrosine kinase family. Curr. Top. Med. Chem. 2002, 2, 1001–1010.
2. Gottesman, M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002, 53, 615–627.
3. Quintieri, L.; Fantin, M.; Vizler, C. Identification of molecular determinants of tumor sensitivity and resistance to anticancer drugs. Adv. Exp. Med. Biol. 2007, 593, 95–104.
4. Deeley, R.G.; Westlake, C.; Cole, S.P. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 2006, 86, 849–899.
5. Jemal, A.; Murray, T.; Ward, E.; Samuels, A.; Tiwari, R.C.; Ghafoor, A.; Feuer, E.J.; Thun, M.J. Cancer statistics, 2005. CA Cancer. J. Clin. 2005, 55, 10–30.
6. Mao, Q.; Unadkat, J.D. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J. 2005, 7, E118–E133.
7. Ambudkar, S.V.; Kim, I.W.; Xia, D.; Sauna, Z.E. The A-Loop, a novel conserved aromatic acid subdomain upstream of the walker a motif in ABC transporters, is critical for ATP binding. FEBS Lett. 2006, 580, 1049–1055.
8. Wu, C.P.; Hsieh, C.H.; Wu, Y.S. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol. Pharm. 2011, 8, 1996–2011.
9. Locher, K.P.; Borths, E. ABC Transporter architecture and mechanism: Implications from the crystal structures of BtuCD and BtuF. FEBS Lett. 2004, 564, 264–268.
10. Higgins, C.F. ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol. 1992, 8, 67–113.
11. Hyde, S.C.; Emsley, P.; Hartshorn, M.J.; Mimmack, M.M.; Gileadi, U.; Pearce, S.R.; Gallagher, M.P.; Gill, D.R.; Hubbard, R.E.; Higgins, C.F. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 1990, 346, 362–365.
12. Tiwari, A.K.; Sodani, K.; Dai, C.L.; Ashby, C.R., Jr.; Chen, Z.S. Revisiting the ABCs of multidrug resistance in cancer chemotherapy. Curr. Pharm. Biotechnol. 2011, 12, 570–594.
13. Dean, M. ABC transporters, drug resistance, and cancer stem cells. J. Mammary Gland Biol. Neoplasia 2009, 14, 3–9.
14. Dean, M.; Annilo, T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu. Rev. Genomics Hum. Genet. 2005, 6, 123–142.
15. Juliano, R.L.; Ling, V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 1976, 455, 152–162.
16. Schinkel, A.H.; Mol, C.A.; Wagenaar, E.; van Deemter, L.; Smit, J.J.; Borst, P. Multidrug resistance and the role of P-Glycoprotein knockout mice. Eur. J. Cancer 1995, 31A, 1295–1298.
17. Gottesman, M.M.; Fojo, T.; Bates, S.E. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer 2002, 2, 48–58.
18. Sarkadi, B.; Homolya, L.; Szakacs, G.; Varadi, A. Human multidrug resistance ABCB and ABCG transporters: Participation in a chemoimmunity defense system. Physiol. Rev. 2006, 86, 1179–1236.
19. Matsuo, K.; Eno, M.L.; Ahn, E.H.; Shahzad, M.M.; Im, D.D.; Rosenshein, N.B.; Sood, A.K. Multidrug resistance gene (MDR-1) and risk of brain metastasis in epithelial ovarian, fallopian tube, and peritoneal cancer. Am. J. Clin. Oncol. 2011, 34, 488–493.
20. Eechoute, K.; Sparreboom, A.; Burger, H.; Franke, R.M.; Schiavon, G.; Verweij, J.; Loos, W.J.; Wiemer, E.A.; Mathijssen, R.H. Drug transporters and imatinib treatment: Implications for clinical practice. Clin. Cancer Res. 2011, 17, 406–415.
21. Gao, Y.J.; Li, B.; Wu, X.Y.; Cui, J.; Han, J.K. Thyroid tumor-initiating cells: Increasing evidence and opportunities for anticancer therapy (Review). Oncol. Rep. 2014, 31, 1035–1042.
22. Gao, B.; Russell, A.; Beesley, J.; Chen, X.Q.; Healey, S.; Henderson, M.; Wong, M.; Emmanuel, C.; Galletta, L.; Johnatty, S.E.; et al. Paclitaxel sensitivity in relation to ABCB1 expression, efflux and single nucleotide polymorphisms in ovarian cancer. Sci. Rep. 2014, 4, doi:10.1038/srep04669.
23. Han, J.Y.; Lim, H.S.; Yoo, Y.K.; Shin, E.S.; Park, Y.H.; Lee, S.Y.; Lee, J.E.; Lee, D.H.; Kim, H.T.; Lee, J.S. Associations of ABCB1, ABCC2, and ABCG2 polymorphisms with irinotecan-pharmacokinetics and clinical outcome in patients with advanced non-small cell lung cancer. Cancer 2007, 110, 138–147.
24. Leonard, G.D.; Fojo, T.; Bates, S.E. The role of ABC transporters in clinical practice. Oncologist 2003, 8, 411–424.
25. Sodani, K.; Patel, A.; Kathawala, R.J.; Chen, Z.S. Multidrug resistance associated proteins in multidrug resistance. Chin. J. Cancer 2012, 31, 58–72.
26. Kruh, G.D.; Belinsky, M.G. The MRP family of drug efflux pumps. Oncogene 2003, 22, 7537–7552.
27. Norris, M.D.; Smith, J.; Tanabe, K.; Tobin, P.; Flemming, C.; Scheffer, G.L.; Wielinga, P.; Cohn, S.L.; London, W.B.; Marshall, G.M.; et al. Expression of multidrug transporter MRP4/ABCC4 is a marker of poor prognosis in neuroblastoma and confers resistance to irinotecan in vitro. Mol. Cancer. Ther. 2005, 4, 547–553.
28. Toh, S.; Wada, M.; Uchiumi, T.; Inokuchi, A.; Makino, Y.; Horie, Y.; Adachi, Y.; Sakisaka, S.; Kuwano, M. Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome. Am. J. Hum. Genet. 1999, 64, 739–746.
29. Ringpfeil, F.; Lebwohl, M.G.; Christiano, A.M.; Uitto, J. Pseudoxanthoma elasticum: Mutations in the MRP6 gene encoding a transmembrane ATP-binding cassette (ABC) transporter. Proc. Natl. Acad. Sci. USA 2000, 97, 6001–6006.
30. Hopper, E.; Belinsky, M.G.; Zeng, H.; Tosolini, A.; Testa, J.R.; Kruh, G.D. Analysis of the structure and expression pattern of MRP7 (ABCC10), a new member of the MRP subfamily. Cancer Lett. 2001, 162, 181–191.
31. Takayanagi, S.; Kataoka, T.; Ohara, O.; Oishi, M.; Kuo, M.T.; Ishikawa, T. Human ATP-binding cassette transporter ABCC10: Expression profile and p53-dependent upregulation. J. Exp. Ther. Oncol. 2004, 4, 239–246.
32. Hopper-Borge, E.A.; Churchill, T.; Paulose, C.; Nicolas, E.; Jacobs, J.D.; Ngo, O.; Kuang, Y.; Grinberg, A.; Westphal, H.; Chen, Z.S.; et al. Contribution of Abcc10 (Mrp7) to in vivo paclitaxel resistance as assessed in Abcc10(-/-) Mice. Cancer Res. 2011, 71, 3649–3657.
33. Chen, Z.S.; Hopper-Borge, E.; Belinsky, M.G.; Shchaveleva, I.; Kotova, E.; Kruh, G.D. Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol. Pharmacol. 2003, 63, 351–358.
34. Bessho, Y.; Oguri, T.; Ozasa, H.; Uemura, T.; Sakamoto, H.; Miyazaki, M.; Maeno, K.; Sato, S.; Ueda, R. ABCC10/MRP7 is associated with vinorelbine resistance in Non-small cell lung cancer. Oncol. Rep. 2009, 21, 263–268.
35. Naramoto, H.; Uematsu, T.; Uchihashi, T.; Doto, R.; Matsuura, T.; Usui, Y.; Uematsu, S.; Li, X.; Takahashi, M.; Yamaoka, M.; et al. Multidrug resistance-Associated protein 7 expression is involved in cross-resistance to docetaxel in salivary gland adenocarcinoma cell lines. Int. J. Oncol. 2007, 30, 393–401.
36. Dabrowska, M.; Sirotnak, F.M. Regulation of transcription of the human MRP7 gene: Characteristics of the basal promoter and identification of tumor-derived transcripts encoding additional 5' end heterogeneity. Gene 2004, 341, 129–139.
37. Robey, R.W.; Polgar, O.; Deeken, J.; To, K.W.; Bates, S.E. ABCG2: Determining its relevance in clinical drug resistance. Cancer Metastasis Rev. 2007, 26, 39–57.
38. Doyle, L.A.; Yang, W.; Abruzzo, L.V.; Krogmann, T.; Gao, Y.; Rishi, A.K.; Ross, D.D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA 1998, 95, 15665–15670.
39. Miyake, K.; Mickley, L.; Litman, T.; Zhan, Z.; Robey, R.; Cristensen, B.; Brangi, M.; Greenberger, L.; Dean, M.; Fojo, T.; et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: Demonstration of homology to ABC transport genes. Cancer Res. 1999, 59, 8–13.
40. Litman, T.; Brangi, M.; Hudson, E.; Fetsch, P.; Abati, A.; Ross, D.D.; Miyake, K.; Resau, J.H.; Bates, S.E. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J. Cell. Sci. 2000, 113, 2011–2021.
41. Maliepaard, M.; van Gastelen, M.A.; Tohgo, A.; Hausheer, F.H.; van Waardenburg, R.C.; de Jong, L.A.; Pluim, D.; Beijnen, J.H.; Schellens, J.H. Circumvention of breast cancer resistance protein (BCRP)-mediated resistance to camptothecins in vitro using non-substrate drugs or the BCRP inhibitor GF120918. Clin. Cancer Res. 2001, 7, 935–941.
42. Schinkel, A.H.; Jonker, J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: An overview. Adv. Drug Deliv. Rev. 2003, 55, 3–29.
43. Merino, G.; Alvarez, A.I.; Pulido, M.M.; Molina, A.J.; Schinkel, A.H.; Prieto, J.G. Breast cancer resistance protein (BCRP/ABCG2) transports fluoroquinolone antibiotics and affects their oral availability, pharmacokinetics, and milk secretion. Drug Metab. Dispos. 2006, 34, 690–695.
44. Ejendal, K.F.; Hrycyna, C.A. Multidrug resistance and cancer: The role of the human ABC transporter ABCG2. Curr. Protein Pept. Sci. 2002, 3, 503–511.
45. Krishnamurthy, P.; Schuetz, J.D. Role of ABCG2/BCRP in biology and medicine. Annu. Rev. Pharmacol. Toxicol. 2006, 46, 381–410.
46. Sharom, F.J.; Yu, X.; Lu, P.; Liu, R.; Chu, J.W.; Szabo, K.; Muller, M.; Hose, C.D.; Monks, A.; Varadi, A.; et al. 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.
47. Nie, S.; Xing, Y.; Kim, G.J.; Simons, J.W. Nanotechnology applications in cancer. Annu. Rev. Biomed. Eng. 2007, 9, 257–288.
48. Basu, S.; Chaudhuri, P.; Sengupta, S. Targeting oncogenic signaling pathways by exploiting nanotechnology. Cell Cycle 2009, 8, 3480–3487.
49. Xue, X.; Liang, X.J. Overcoming drug efflux-based multidrug resistance in cancer with nanotechnology. Chin. J. Cancer 2012, 31, 100–109.
50. Shi, Z.; Peng, X.X.; Kim, I.W.; Shukla, S.; Si, Q.S.; Robey, R.W.; Bates, S.E.; Shen, T.; Ashby, C.R., Jr.; Fu, L.W.; 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. 2007, 67, 11012–11020.
51. Ludwig, J.A.; Szakacs, G.; Martin, S.E.; Chu, B.F.; Cardarelli, C.; Sauna, Z.E.; Caplen, N.J.; Fales, H.M.; Ambudkar, S.V.; Weinstein, J.N.; et al. Selective toxicity of NSC73306 in MDR1-positive cells as a new strategy to circumvent multidrug resistance in cancer. Cancer Res. 2006, 66, 4808–4815.
52. Krause, D.S.; van Etten, R.A. Tyrosine kinases as targets for cancer therapy. N. Engl. J. Med. 2005, 353, 172–187.
53. Faivre, S.; Djelloul, S.; Raymond, E. New paradigms in anticancer therapy: Targeting multiple signaling pathways with kinase inhibitors. Semin. Oncol. 2006, 33, 407–420.
54. Luke, J.J.; Hodi, F.S. Vemurafenib and BRAF inhibition: A new class of treatment for metastatic melanoma. Clin. Cancer Res. 2012, 18, 9–14.
55. ®), a BRAF inhibitor, modulates ABCB1-, ABCG2-, and ABCC10-mediated multidrug resistance. J. Cancer Res. Updates 2013, 2, 306–317.
56. Dai, C.L.; Tiwari, A.K.; Wu, C.P.; Su, X.D.; Wang, S.R.; Liu, D.G.; Ashby, C.R., Jr.; Huang, Y.; Robey, R.W.; Liang, Y.J.; 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. 2008, 68, 7905–7914.
57. Shen, T.; Kuang, Y.H.; Ashby, C.R.; Lei, Y.; Chen, A.; Zhou, Y.; Chen, X.; Tiwari, A.K.; Hopper-Borge, E.; Ouyang, J. et al. Imatinib and nilotinib reverse multidrug resistance in cancer cells by inhibiting the efflux activity of the MRP7 (ABCC10). PLoS One 2009, 4, e7520.
58. Tiwari, A.K.; Sodani, K.; Wang, S.R.; Kuang, Y.H.; Ashby, C.R., Jr.; Chen, X.; Chen, Z.S. Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters. Biochem. Pharmacol. 2009, 78, 153–161.
59. Tiwari, A.K.; Sodani, K.; Dai, C.L.; Abuznait, A.H.; Singh, S.; Xiao, Z.J.; Patel, A.; Talele, T.T.; Fu, L.; Kaddoumi, A. et al. Nilotinib potentiates anticancer drug sensitivity in murine ABCB1-, ABCG2-, and ABCC10-multidrug resistance xenograft models. Cancer Lett. 2013, 328, 307–317.
60. Kathawala, R.J.; Sodani, K.; Chen, K.; Patel, A.; Abuznait, A.H.; Anreddy, N.; Sun, Y.L.; Kaddoumi, A.; Ashby, C.R., Jr.; Chen, Z.S. Masitinib antagonizes ATP-binding cassette subfamily C member 10-mediated paclitaxel resistance: A preclinical study. Mol. Cancer. Ther. 2014, 13, 714–723.
61. Sodani, K.; Patel, A.; Anreddy, N.; Singh, S.; Yang, D.H.; Kathawala, R.J.; Kumar, P.; Talele, T.T.; Chen, Z.S. Telatinib reverses chemotherapeutic multidrug resistance mediated by ABCG2 efflux transporter in vitro and in vivo. Biochem. Pharmacol. 2014, 89, 52–61.
62. Zhang, H.; Kathawala, R.J.; Wang, Y.J.; Zhang, Y.K.; Patel, A.; Shukla, S.; Robey, R.W.; Talele, T.T.; Ashby, C.R., Jr.; Ambudkar, S.V. et al. Linsitinib (OSI-906) antagonizes ATP-binding cassette subfamily G member 2 and subfamily C member 10-mediated drug resistance. Int. J. Biochem. Cell Biol. 2014, 51, 111–119.
63. Zhang, H.; Wang, Y.J.; Zhang, Y.K.; Wang, D.S.; Kathawala, R.J.; Patel, A.; Talele, T.T.; Chen, Z.S.; Fu, L.W. AST1306, a potent EGFR inhibitor, antagonizes ATP-binding cassette subfamily G member 2-mediated multidrug resistance. Cancer Lett. 2014, 350, 61–68.
64. Zhang, H.; Zhang, Y.K.; Wang, Y.J.; Kathawala, R.J.; Patel, A.; Zhu, H.; Sodani, K.; Talele, T.T.; Ambudkar, S.V.; Chen, Z.S. et al. WHI-P154 enhances the chemotherapeutic effect of anticancer agents in ABCG2-overexpressing cells. Cancer Sci. 2014, 105, 1071–1078.
65. Wang, Y.J.; Kathawala, R.J.; Zhang, Y.K.; Patel, A.; Kumar, P.; Shukla, S.; Fung, K.L.; Ambudkar, S.V.; Talele, T.T.; Chen, Z.S. Motesanib (AMG706), a potent multikinase inhibitor, antagonizes multidrug resistance by inhibiting the efflux activity of the ABCB1. Biochem. Pharmacol. 2014, 90, 367–378.
66. Aller, S.G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P.M.; Trinh, Y.T.; Zhang, Q.; Urbatsch, I.L. et al. Structure of P-Glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323, 1718–1722.
67. Nicolle, E.; Boumendjel, A.; Macalou, S.; Genoux, E.; Ahmed-Belkacem, A.; Carrupt, P.A.; di Pietro, A. QSAR analysis and molecular modeling of ABCG2-specific inhibitors. Adv. Drug Deliv. Rev. 2009, 61, 34–46.
68. Crivori, P.; Reinach, B.; Pezzetta, D.; Poggesi, I. Computational models for identifying potential P-Glycoprotein substrates and inhibitors. Mol. Pharm. 2006, 3, 33–44.
69. Pajeva, I.K.; Globisch, C.; Wiese, M. Combined pharmacophore modeling, docking, and 3D QSAR studies of ABCB1 and ABCC1 transporter inhibitors. ChemMedChem 2009, 4, 1883–1896.
70. Xie, H.; Lin, L.; Tong, L.; Jiang, Y.; Zheng, M.; Chen, Z.; Jiang, X.; Zhang, X.; Ren, X.; Qu, W. et al. AST1306, a novel irreversible inhibitor of the epidermal growth factor receptor 1 and 2, exhibits antitumor activity both in vitro and in vivo. PLoS One 2011, 6, e21487.
71. Zhang, J.; Cao, J.; Li, J.; Zhang, Y.; Chen, Z.; Peng, W.; Sun, S.; Zhao, N.; Wang, J.; Zhong, D. et al. A phase I study of AST1306, a novel irreversible EGFR and HER2 kinase inhibitor, in patients with advanced solid tumors. J. Hematol. Oncol. 2014, 7, 22.
72. Normanno, N.; de Luca, A.; Bianco, C.; Strizzi, L.; Mancino, M.; Maiello, M.R.; Carotenuto, A.; de Feo, G.; Caponigro, F.; Salomon, D.S. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006, 366, 2–16.
73. Mulvihill, M.J.; Cooke, A.; Rosenfeld-Franklin, M.; Buck, E.; Foreman, K.; Landfair, D.; O’Connor, M.; Pirritt, C.; Sun, Y.; Yao, Y.; et al. Discovery of OSI-906: A selective and orally efficacious dual inhibitor of the IGF-1 receptor and insulin receptor. Future Med. Chem. 2009, 1, 1153–1171.
74. McKinley, E.T.; Bugaj, J.E.; Zhao, P.; Guleryuz, S.; Mantis, C.; Gokhale, P.C.; Wild, R.; Manning, H.C. 18FDG-PET Predicts pharmacodynamic response to OSI-906, a dual IGF-1R/IR inhibitor, in preclinical mouse models of lung cancer. Clin. Cancer Res. 2011, 17, 3332–3340.
75. Le Cesne, A.; Blay, J.Y.; Bui, B.N.; Bouche, O.; Adenis, A.; Domont, J.; Cioffi, A.; Ray-Coquard, I.; Lassau, N.; Bonvalot, S.; et al. Phase II study of oral masitinib mesilate in imatinib-naive patients with locally advanced or metastatic gastro-intestinal stromal tumour (GIST). Eur. J. Cancer 2010, 46, 1344–1351.
76. Mitry, E.; Hammel, P.; Deplanque, G.; Mornex, F.; Levy, P.; Seitz, J.F.; Moussy, A.; Kinet, J.P.; Hermine, O.; Rougier, P.; et al. Safety and activity of masitinib in combination with gemcitabine in patients with advanced pancreatic cancer. Cancer Chemother. Pharmacol. 2010, 66, 395–403.
77. Georgin-Lavialle, S.; Lhermitte, L.; Suarez, F.; Yang, Y.; Letard, S.; Hanssens, K.; Feger, F.; Renand, A.; Brouze, C.; Canioni, D. et al. Mast cell leukemia: Identification of a new C-Kit mutation, dup(501–502), and response to masitinib, a C-Kit tyrosine kinase inhibitor. Eur. J. Haematol. 2012, 89, 47–52.
78. Kathawala, R.J.; Chen, J.J.; Zhang, Y.K.; Wang, Y.J.; Patel, A.; Wang, D.S.; Talele, T.T.; Ashby, C.R., Jr.; Chen, Z.S. Masitinib antagonizes ATP-binding cassette subfamily G member 2-mediated multidrug resistance. Int. J. Oncol. 2014, 44, 1634–1642.
79. Polverino, A.; Coxon, A.; Starnes, C; Diaz, Z.; DeMelfi, T.; Wang, L.; Bready, J.; Estrada, J.; Cattley, R.; Kaufman, S. et al. AMG 706, an oral, multikinase inhibitor that selectively targets vascular endothelial growth factor, platelet-derived growth factor, and kit receptors, potently inhibits angiogenesis and induces regression in tumor xenografts. Cancer Res. 2006, 66, 8715-8721.
80. Gora-Tybor, J.; Robak, T. Targeted drugs in chronic myeloid leukemia. Curr. Med. Chem. 2008, 15, 3036-3051.
81. Shah, N.P.; Nicoll, J.M.; Nagar, B.; Gorre, M.E.; Paquette, R.L.; Kuriyan, J.; Sawyers, C.L. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2002, 2, 117-125.
82. Langenberg, M.H.; Witteveen, P.O.; Roodhart, J.M.; Verheul, H.M.; Mergui-Roelvink, M.; van der Sar, J.; Brendel, E.; Laferriere, N.; Schellens, J.H.; Voest, E.E. Phase I evaluation of telatinib, a vascular endothelial growth factor receptor tyrosine kinase inhibitor, in combination with irinotecan and capecitabine in patients with advanced solid tumors. Clin. Cancer Res. 2010, 16, 2187-2197.
83. Sudbeck, E.A.; Ghosh, S.; Liu, X.P.; Zheng, Y.; Myers, D.E.; Uckun, F.M. Tyrosine kinase inhibitors against EGF receptor-positive malignancies. Methods Mol. Biol. 2001, 166, 193-218.
84. Marzec, M.; Kasprzycka, M.; Ptasznik, A.; Wlodarski, P.; Zhang, Q.; Odum, N.; Wasik, M.A. Inhibition of ALK enzymatic activity in T-cell lymphoma cells induces apoptosis and suppresses proliferation and STAT3 phosphorylation independently of Jak3. Lab. Invest. 2005, 85, 1544-1554.
85. Stewart, C.F.; Leggas, M.; Schuetz, J.D.; Panetta, J.C.; Cheshire, P.J.; Peterson, J.; Daw, N.; Jenkins, J.J., III; Gilbertson, R.; Germain, G.S. et al. Gefitinib enhances the antitumor activity and oral bioavailability of irinotecan in mice. Cancer Res. 2004, 64, 7491-7499.
86. Nakamura, Y.; Oka, M.; Soda, H.; Shiozawa, K.; Yoshikawa, M.; Itoh, A.; Ikegami, Y.; Tsurutani, J.; Nakatomi, K.; Kitazaki, T. et al. Gefitinib (–Iressaߞ, ZD1839), an epidermal growth factor receptor tyrosine kinase inhibitor, reverses breast cancer resistance protein/ ABCG2-mediated drug resistance. Cancer Res. 2005, 65, 1541-1546.
87. Chen, K.G.; Sikic, B.I. Molecular pathways: Regulation and therapeutic implications of multidrug resistance. Clin. Cancer Res. 2012, 18, 1863-1869.
88. Sikic, B.I.; Fisher, G.A.; Lum, B.L.; Halsey, J.; Beketic-Oreskovic, L.; Chen, G. Modulation and prevention of multidrug resistance by inhibitors of P-Glycoprotein. Cancer Chemother. Pharmacol. 1997, 40, S13-S19.
89. Yahanda, A.M.; Alder, K.M.; Fisher, G.A.; Brophy, N.A.; Halsey, J.; Hardy, R.I.; Gosland, M.P.; Lum, B.L.; Sikic, B.I. Phase I trial of etoposide with cyclosporine as a modulator of multidrug resistance. J. Clin. Oncol. 1992, 10, 1624-1634.
90. Lum, B.L.; Kaubisch, S.; Yahanda, A.M.; Adler, K.M.; Jew, L.; Ehsan, M.N.; Brophy, N.A.; Halsey, J.; Gosland, M.P.; Sikic, B.I. Alteration of etoposide pharmacokinetics and pharmacodynamics by cyclosporine in a phase I trial to modulate multidrug resistance. J. Clin. Oncol. 1992, 10, 1635-1642.
91. Bartlett, N.L.; Lum, B.L.; Fisher, G.A.; Brophy, N.A.; Ehsan, M.N.; Halsey, J.; Sikic, B.I. Phase I trial of doxorubicin with cyclosporin as a modulator of multidrug resistance. J. Clin. Oncol. 1994, 12, 835-842.
92. Advani, R.; Fisher, G.A.; Lum, B.L.; Hausdorff, J.; Halsey, J.; Litchman, M.; Sikic, B.I. A phase I trial of doxorubicin, paclitaxel, and valspodar (PSC 833), a modulator of multidrug resistance. Clin. Cancer Res. 2001, 7, 1221-1229.
93. Baer, M.R.; George, S.L.; Dodge, R.K.; O'Loughlin, K.L.; Minderman, H.; Caligiuri, M.A.; Anastasi, J.; Powell, B.L.; Kolitz, J.E.; Schiffer, C.A. et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and leukemia group B study 9720. Blood 2002, 100, 1224-1232.
94. List, A.F.; Kopecky, K.J.; Willman, C.L.; Head, D.R.; Persons, D.L.; Slovak, M.L.; Dorr, R.; Karanes, C; Hynes, H.E.; Doroshow, J.H. et al. Benefit of cyclosporine modulation of drug resistance in patients with poor-risk acute myeloid leukemia: A southwest oncology group study. Blood 2001, 98, 3212-3220.
95. Liu Yin, J.A.; Wheatley, K.; Rees, J.K.; Burnett, A.K.; UK MRC Adult Leukemia Working Party. Comparison of –Sequentialߞ versus –Standardߞ chemotherapy as re-induction treatment, with or without cyclosporine, in refractory/relapsed acute myeloid leukaemia (AML): Results of the UK medical research council AML-R trial. Br. J. Haematol. 2001, 113, 713-726.
96. Cripe, L.D.; Uno, H.; Paietta, E.M.; Litzow, M.R.; Ketterling, R.P.; Bennett, J.M.; Rowe, J.M.; Lazarus, H.M.; Luger, S.; Tallman, M.S. Zosuquidar, a novel modulator of P-Glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: A randomized, Placebo-controlled trial of the eastern Cooperative Oncology Group 3999. Blood 2010, 116, 4077-4085.
97. Qadir, M.; O’Loughlin, K.L.; Fricke, S.M.; Williamson, N.A.; Greco, W.R.; Minderman, H.; Baer, M.R. Cyclosporin A is a broad-spectrum multidrug resistance modulator. Clin. Cancer Res. 2005, 11, 2320-2326.
98. Matsubara, H.; Watanabe, M.; Imai, T.; Yui, Y.; Mizushima, Y.; Hiraumi, Y.; Kamitsuji, Y.; Watanabe, K; Nishijo, K; Toguchida, J. et al. Involvement of extracellular signal-regulated kinase activation in human osteosarcoma cell resistance to the histone deacetylase inhibitor FK228 [(1S,4S,7Z,10S,16E,21R)-7-Ethylidene-4,21-Bis(Propan-2-Yl)-2-Oxa-12,13-Dithia-5,8,20,23-Te traazabicyclo[8.7.6]Tricos-16-Ene-3,6,9,19,22-Pentone. J. Pharmacol. Exp. Ther. 2009, 328, 839-848.
99. Tabe, Y.; Konopleva, M.; Contractor, R.; Munsell, M.; Schober, W.D.; Jin, L.; Tsutsumi-Ishii, Y.; Nagaoka, I.; Igari, J.; Andreeff, M. Up-regulation of MDR1 and induction of doxorubicin resistance by histone deacetylase inhibitor depsipeptide (FK228) and ATRA in acute promyelocytic leukemia cells. Blood 2006, 107, 1546-1554.
100. Van den Heuvel-Eibrink, M.M.; Wiemer, E.A.; Prins, A.; Meijerink, J.P.; Vossebeld, P.J.; van der Holt, B.; Pieters, R.; Sonneveld, P. Increased expression of the breast cancer resistance protein (BCRP) in relapsed or refractory acute myeloid leukemia (AML). Leukemia 2002, 16, 833-839.
101. Tang, S.C.; Lagas, J.S.; Lankheet, N.A.; Poller, B.; Hillebrand, M.J.; Rosing, H.; Beijnen, J.H.; Schinkel, A.H. Brain accumulation of sunitinib is restricted by P-Glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by oral elacridar and sunitinib coadministration. Int. J. Cancer 2012, 130, 223–233.
102. Plasschaert, S.L.; van der Kolk, D.M.; de Bont, E.S.; Kamps, W.A.; Morisaki, K.; Bates, S.E.; Scheffer, G.L.; Scheper, R.J.; Vellenga, E.; de Vries, E.G. The role of breast cancer resistance protein in acute lymphoblastic leukemia. Clin. Cancer Res. 2003, 9, 5171–5177.
103. Sauerbrey, A.; Sell, W.; Steinbach, D.; Voigt, A.; Zintl, F. Expression of the BCRP gene (ABCG2/MXR/ABCP) in childhood acute lymphoblastic leukaemia. Br. J. Haematol. 2002, 118, 147–150.
104. Jordanides, N.E.; Jorgensen, H.G.; Holyoake, T.L.; Mountford, J.C. Functional ABCG2 is overexpressed on primary CML CD34+ cells and is Inhibited by imatinib mesylate. Blood 2006, 108, 1370–1373.
105. Kim, J.E.; Singh, R.R.; Cho-Vega, J.H.; Drakos, E.; Davuluri, Y.; Khokhar, F.A.; Fayad, L.; Medeiros, L.J.; Vega, F. Sonic hedgehog signaling proteins and ATP-binding cassette G2 are aberrantly expressed in diffuse large B-Cell lymphoma. Mod. Pathol. 2009, 22, 1312–1320.
106. Szczuraszek, K.; Materna, V.; Halon, A.; Mazur, G.; Wrobel, T.; Kuliczkowski, K.; Maciejczyk, A.; Zabel, M.; Drag, M.; Dietel, M. et al. Positive correlation between cyclooxygenase-2 and ABC-transporter expression in non-hodgkin’s lymphomas. Oncol. Rep. 2009, 22, 1315–1323.
107. Kim, Y.H.; Ishii, G.; Goto, K.; Ota, S.; Kubota, K.; Murata, Y.; Mishima, M.; Saijo, N.; Nishiwaki, Y.; Ochiai, A. Expression of breast cancer resistance protein is associated with a poor clinical outcome in patients with small-cell lung cancer. Lung Cancer 2009, 65, 105–111.
108. Rijavec, M.; Silar, M.; Triller, N.; Kern, I.; Cegovnik, U.; Kosnik, M.; Korosec, P. Expressions of topoisomerase IIalpha and BCRP in metastatic cells are associated with overall survival in small cell lung cancer patients. Pathol. Oncol. Res. 2011, 17, 691–696.
109. Yamada, A.; Ishikawa, T.; Ota, I.; Kimura, M.; Shimizu, D.; Tanabe, M.; Chishima, T.; Sasaki, T.; Ichikawa, Y.; Morita, S. et al. High expression of ATP-binding cassette transporter ABCC11 in breast tumors is associated with aggressive subtypes and low disease-free survival. Breast Cancer Res. Treat. 2013, 137, 773–782.
110. Hlavata, I.; Mohelnikova-Duchonova, B.; Vaclavikova, R.; Liska, V.; Pitule, P.; Novak, P.; Bruha, J.; Vycital, O.; Holubec, L.; Treska, V. et al. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis 2012, 27, 187–196.
111. Kunicka, T.; Soucek, P. Importance of ABCC1 for cancer therapy and prognosis. Drug Metab. Rev. 2014, 46, 325–342.
112. Young, L.C.; Campling, B.G.; Cole, S.P.; Deeley, R.G.; Gerlach, J.H. Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: Correlation of protein levels with drug response and messenger RNA levels. Clin. Cancer Res. 2001, 7, 1798–1804.
113. Zalcberg, J.; Hu, X.F.; Slater, A.; Parisot, J.; El-Osta, S.; Kantharidis, P.; Chou, S.T.; Parkin, J.D. MRP1 Not MDR1 Gene expression is the predominant mechanism of acquired multidrug resistance in two prostate carcinoma cell lines. Prostate Cancer Prostatic Dis. 2000, 3, 66–75.
114. Chauhan, P.S.; Bhushan, B.; Singh, L.C.; Mishra, A.K.; Saluja, S.; Mittal, V.; Gupta, D.K.; Kapur, S. Expression of genes related to multiple drug resistance and apoptosis in acute leukemia: Response to induction chemotherapy. Exp. Mol. Pathol. 2012, 92, 44–49.
115. Cui, Y.; Konig, J.; Buchholz, J.K.; Spring, H.; Leier, I.; Keppler, D. Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. 1999, 55, 929–937.
116. Huisman, M.T.; Chhatta, A.A.; van Tellingen, O.; Beijnen, J.H.; Schinkel, A.H. MRP2 (ABCC2) transports taxanes and confers paclitaxel resistance and both processes are stimulated by probenecid. Int. J. Cancer 2005, 116, 824–829.
117. Guminski, A.D.; Balleine, R.L.; Chiew, Y.E.; Webster, L.R.; Tapner, M.; Farrell, G.C.; Harnett, P.R.; Defazio, A. MRP2 (ABCC2) and cisplatin sensitivity in hepatocytes and human ovarian carcinoma. Gynecol. Oncol. 2006, 100, 239–246.
118. Zelcer, N.; Saeki, T.; Reid, G.; Beijnen, J.H.; Borst, P. Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J. Biol. Chem. 2001, 276, 46400–46407.
119. Zeng, H.; Chen, Z.S.; Belinsky, M.G.; Rea, P.A.; Kruh, G.D. Transport of methotrexate (MTX) and folates by multidrug resistance protein (MRP) 3 and MRP1: Effect of polyglutamylation on MTX transport. Cancer Res. 2001, 61, 7225–7232.
120. Chen, Z.S.; Lee, K.; Kruh, G.D. Transport of cyclic nucleotides and estradiol 17-Beta-D-Glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J. Biol. Chem. 2001, 276, 33747–33754.
121. Tian, Q.; Zhang, J.; Tan, T.M.; Chan, E.; Duan, W.; Chan, S.Y.; Boelsterli, U.A.; Ho, P.C.; Yang, H.; Bian, J.S. et al. Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm. Res. 2005, 22, 1837–1853.
122. Pratt, S.; Shepard, R.L.; Kandasamy, R.A.; Johnston, P.A.; Perry, W., III; Dantzig, A.H. The multidrug resistance protein 5 (ABCC5) confers resistance to 5-fluorouracil and transports its monophosphorylated metabolites. Mol. Cancer. Ther. 2005, 4, 855–863.
123. Belinsky, M.G.; Chen, Z.S.; Shchaveleva, I.; Zeng, H.; Kruh, G.D. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res. 2002, 62, 6172–6177.
124. Wang, P.; Zhang, Z.; Gao, K.; Deng, Y.; Zhao, J.; Liu, B.; Li, X. Expression and clinical significance of ABCC10 in the patients with non-small cell lung cancer (in Chinese). Zhongguo Fei Ai Za Zhi 2009, 12, 875–878.
125. Hu, S.; Niu, H.; Inaba, H.; Orwick, S.; Rose, C.; Panetta, J.C.; Yang, S.; Pounds, S.; Fan, Y.; Calabrese, C. et al. Activity of the multikinase inhibitor sorafenib in combination with cytarabine in acute myeloid leukemia. J. Natl. Cancer Inst. 2011, 103, 893–905.
126. Walle, T.; Walle, U.K.; Kumar, G.N.; Bhalla, K.N. Taxol metabolism and disposition in cancer patients. Drug Metab. Dispos. 1995, 23, 506–512.
127. Sparreboom, A.; van Asperen, J.; Mayer, U.; Schinkel, A.H.; Smit, J.W.; Meijer, D.K.; Borst, P.; Nooijen, W.J.; Beijnen, J.H.; van Tellingen, O. Limited oral bioavailability and active epithelial excretion of paclitaxel (Taxol) caused by P-Glycoprotein in the intestine. Proc. Natl. Acad. Sci. USA 1997, 94, 2031–2035.
128. Green, H.; Soderkvist, P.; Rosenberg, P.; Horvath, G.; Peterson, C. ABCB1 G1199A polymorphism and ovarian cancer response to paclitaxel. J. Pharm. Sci. 2008, 97, 2045–2048.
129. Green, H.; Soderkvist, P.; Rosenberg, P.; Horvath, G.; Peterson, C. Mdr-1 single nucleotide polymorphisms in ovarian cancer tissue: G2677T/A correlates with response to paclitaxel chemotherapy. Clin. Cancer Res. 2006, 12, 854–859.
130. Sissung, T.M.; Mross, K.; Steinberg, S.M.; Behringer, D.; Figg, W.D.; Sparreboom, A.; Mielke, S. Association of ABCB1 genotypes with paclitaxel-mediated peripheral neuropathy and neutropenia. Eur. J. Cancer 2006, 42, 2893–2896.
131. Nakajima, M.; Fujiki, Y.; Kyo, S.; Kanaya, T.; Nakamura, M.; Maida, Y.; Tanaka, M.; Inoue, M.; Yokoi, T. Pharmacokinetics of paclitaxel in ovarian cancer patients and genetic polymorphisms of CYP2C8, CYP3A4, and MDR1. J. Clin. Pharmacol. 2005, 45, 674–682.
132. Henningsson, A.; Marsh, S.; Loos, W.J.; Karlsson, M.O.; Garsa, A.; Mross, K.; Mielke, S.; Vigano, L.; Locatelli, A.; Verweij, J. et al. Association of CYP2C8, CYP3A4, CYP3A5, and ABCB1 polymorphisms with the pharmacokinetics of paclitaxel. Clin. Cancer Res. 2005, 11, 8097–8104.
133. Grimm, C.; Polterauer, S.; Zeillinger, R.; Tong, D.; Heinze, G.; Wolf, A.; Natter, C.; Reinthaller, A.; Hefler, L.A. Two multidrug-resistance (ABCB1) gene polymorphisms as prognostic parameters in women with ovarian cancer. Anticancer Res. 2010, 30, 3487–3491.
134. Marsh, S.; Paul, J.; King, C.R.; Gifford, G.; McLeod, H.L.; Brown, R. Pharmacogenetic assessment of toxicity and outcome after platinum plus taxane chemotherapy in ovarian cancer: The Scottish randomised trial in ovarian cancer. J. Clin. Oncol. 2007, 25, 4528–4535.
135. Wojnowski, L.; Kulle, B.; Schirmer, M.; Schluter, G.; Schmidt, A.; Rosenberger, A.; Vonhof, S.; Bickeboller, H.; Toliat, M.R.; Suk, E.K. et al. NAD(P)H oxidase and multidrug resistance protein genetic polymorphisms are associated with doxorubicin-induced cardiotoxicity. Circulation 2005, 112, 3754–3762.
136. Colombo, S.; Soranzo, N.; Rotger, M.; Sprenger, R.; Bleiber, G.; Furrer, H.; Buclin, T.; Goldstein, D.; Decosterd, L.; Telenti, A. et al. Influence of ABCB1, ABCC1, ABCC2, and ABCG2 haplotypes on the cellular exposure of nelfinavir in vivo. Pharmacogenet. Genomics 2005, 15, 599–608.
137. Kartenbeck, J.; Leuschner, U.; Mayer, R.; Keppler, D. Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in dubin-johnson syndrome. Hepatology 1996, 23, 1061–1066.
138. Gradhand, U.; Kim, R.B. Pharmacogenomics of MRP transporters (ABCC1–5) and BCRP (ABCG2). Drug Metab. Rev. 2008, 40, 317–354.
139. Kato, T.; Hamada, A.; Mori, S.; Saito, H. Genetic polymorphisms in metabolic and cellular transport pathway of methotrexate impact clinical outcome of methotrexate monotherapy in Japanese patients with rheumatoid arthritis. Drug Metab. Pharmacokinet. 2012, 27, 192–199.
140. Pushpakom, S.P.; Liptrott, N.J.; Rodriguez-Novoa, S.; Labarga, P.; Soriano, V.; Albalater, M.; Hopper-Borge, E.; Bonora, S.; di Perri, G.; Back, D.J. et al. Genetic variants of ABCC10, a novel tenofovir transporter, are associated with kidney tubular dysfunction. J. Infect. Dis. 2011, 204, 145–153.
141. Liptrott, N.J.; Pushpakom, S.; Wyen, C.; Fatkenheuer, G.; Hoffmann, C.; Mauss, S.; Knechten, H.; Brockmeyer, N.H.; Hopper-Borge, E.; Siccardi, M. et al. Association of ABCC10 polymorphisms with nevirapine plasma concentrations in the german competence network for HIV/AIDS. Pharmacogenet. Genomics 2012, 22, 10–19.
142. Ciccacci, C.; di Fusco, D.; Marazzi, M.C.; Liotta, G.; Palombi, L.; Novelli, G.; Borgiani, P. ABCC10 rs2125739 polymorphism and nevirapine-induced hepatotoxicity: Lack of association in a population from mozambique. Pharmacogenet. Genomics 2013, 23, 38–39.
143. Cusatis, G.; Sparreboom, A. Pharmacogenomic importance of ABCG2. Pharmacogenomics 2008, 9, 1005–1009.
144. Cusatis, G.; Gregorc, V.; Li, J.; Spreafico, A.; Ingersoll, R.G.; Verweij, J.; Ludovini, V.; Villa, E.; Hidalgo, M.; Sparreboom, A. et al. Pharmacogenetics of ABCG2 and adverse reactions to gefitinib. J. Natl. Cancer Inst. 2006, 98, 1739–1742.
145. Zamboni, W.C.; Ramanathan, R.K.; McLeod, H.L.; Mani, S.; Potter, D.M.; Strychor, S.; Maruca, L.J.; King, C.R.; Jung, L.L.; Parise, R.A. et al. Disposition of 9-nitrocamptothecin and its 9-aminocamptothecin metabolite in relation to ABC transporter genotypes. Invest. New Drugs 2006, 24, 393–401.
146. Sparreboom, A.; Gelderblom, H.; Marsh, S.; Ahluwalia, R.; Obach, R.; Principe, P.; Twelves, C.; Verweij, J.; McLeod, H.L. Diflomotecan pharmacokinetics in relation to ABCG2 421C > A genotype. Clin. Pharmacol. Ther. 2004, 76, 38–44.
147. Zhou, Q.; Sparreboom, A.; Tan, E.H.; Cheung, Y.B.; Lee, A.; Poon, D.; Lee, E.J.; Chowbay, B. Pharmacogenetic profiling across the irinotecan pathway in asian patients with cancer. Br. J. Clin. Pharmacol. 2005, 59, 415–424.
148. Zhang, W.; Yu, B.N.; He, Y.J.; Fan, L.; Li, Q.; Liu, Z.Q.; Wang, A.; Liu, Y.L.; Tan, Z.R.; Jiang, F. et al. Role of BCRP 421C > A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin. Chim. Acta 2006, 373, 99–103.
149. Urquhart, B.L.; Ware, J.A.; Tirona, R.G.; Ho, R.H.; Leake, B.F.; Schwarz, U.I.; Zaher, H.; Palandra, J.; Gregor, J.C.; Dresser, G.K. et al. Breast cancer resistance protein (ABCG2) and drug disposition: Intestinal expression, polymorphisms and sulfasalazine as an in vivo probe. Pharmacogenet. Genomics 2008, 18, 439–448.
150. Yamasaki, Y.; Ieiri, I.; Kusuhara, H.; Sasaki, T.; Kimura, M.; Tabuchi, H.; Ando, Y.; Irie, S.; Ware, J.; Nakai, Y. et al. Pharmacogenetic characterization of sulfasalazine disposition based on NAT2 and ABCG2 (BCRP) gene polymorphisms in humans. Clin. Pharmacol. Ther. 2008, 84, 95–103.
151. Sparreboom, A.; Loos, W.J.; Burger, H.; Sissung, T.M.; Verweij, J.; Figg, W.D.; Nooter, K.; Gelderblom, H. Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol. Ther. 2005, 4, 650–658.
152. Lal, S.; Wong, Z.W.; Sandanaraj, E.; Xiang, X.; Ang, P.C.; Lee, E.J.; Chowbay, B. Influence of ABCB1 and ABCG2 polymorphisms on doxorubicin disposition in Asian breast cancer patients. Cancer Sci. 2008, 99, 816–823.
153. Gardner, E.R.; Burger, H.; van Schaik, R.H.; van Oosterom, A.T.; de Bruijn, E.A.; Guetens, G.; Prenen, H.; de Jong, F.A.; Baker, S.D.; Bates, S.E.; et al. Association of enzyme and transporter genotypes with the pharmacokinetics of imatinib. Clin. Pharmacol. Ther. 2006, 80, 192–201.
154. Ieiri, I.; Suwannakul, S.; Maeda, K.; Uchimaru, H.; Hashimoto, K.; Kimura, M.; Fujino, H.; Hirano, M.; Kusuhara, H.; Irie, S.; et al. SLCO1B1 (OATP1B1, an uptake transporter) and ABCG2 (BCRP, an efflux transporter) variant alleles and pharmacokinetics of pitavastatin in healthy volunteers. Clin. Pharmacol. Ther. 2007, 82, 541–547.
155. Yoshioka, S.; Katayama, K.; Okawa, C.; Takahashi, S.; Tsukahara, S.; Mitsuhashi, J.; Sugimoto, Y. The identification of two germ-line mutations in the human breast cancer resistance protein gene that result in the expression of a low/non-functional protein. Pharm. Res. 2007, 24, 1108–1117.
156. Rudin, C.M.; Liu, W.; Desai, A.; Karrison, T.; Jiang, X.; Janisch, L.; Das, S.; Ramirez, J.; Poonkuzhali, B.; Schuetz, E.; et al. Pharmacogenomic and pharmacokinetic determinants of erlotinib toxicity. J. Clin. Oncol. 2008, 26, 1119–1127.
157. Poonkuzhali, B.; Lamba, J.; Strom, S.; Sparreboom, A.; Thummel, K.; Watkins, P.; Schuetz, E. Association of breast cancer resistance protein/ABCG2 phenotypes and novel promoter and intron 1 single nucleotide polymorphisms. Drug Metab. Dispos. 2008, 36, 780–795.
158. Innocenti, F.; Kroetz, D.L.; Schuetz, E.; Dolan, M.E.; Ramirez, J.; Relling, M.; Chen, P.; Das, S.; Rosner, G.L.; Ratain, M.J. Comprehensive pharmacogenetic analysis of irinotecan neutropenia and pharmacokinetics. J. Clin. Oncol. 2009, 27, 2604–2614.
159. Cecchin, E.; D’Andrea, M.; Lonardi, S.; Zanusso, C.; Pella, N.; Errante, D.; de Mattia, E.; Polesel, J.; Innocenti, F.; Toffoli, G. A prospective validation pharmacogenomic study in the adjuvant setting of colorectal cancer patients treated with the 5-Fluorouracil/Leucovorin/Oxaliplatin (FOLFOX4) regimen. Pharmacogenomics J. 2013, 13, 403–409.