ARRY-334543 reverses multidrug resistance by antagonizing the activity of atp-binding cassette subfamily g member 2

Journal of Cellular Biochemistry

Volumn 115, Issue 8, 2014, Pages 1381-1391

  Wang, De Shen ^a,b   Patel, Atish ^b   Sim, Hong May ^c   Zhang, Yun Kai ^b   Wang, Yi Jun ^b   Kathawala, Rishil J ^b   Zhang, Hui ^b   Talele, Tanaji T ^b   Ambudkar, Suresh V ^c   Xu, Rui Hua ^a   Chen, Zhe Sheng ^b  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b ST JOHN'S UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

abcg2; ARRY 334543; lung cancer; multidrug resistance; tyrosine kinase inhibitor

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; FIRTECAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOXANTRONE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 7; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN KINASE B; VARLITINIB; ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; ARRY-334543; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; ONCOPROTEIN; PACLITAXEL; PROTEIN BINDING; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; THIAZOLE DERIVATIVE; TUMOR PROTEIN;

ARTICLE; CHEMOSENSITIVITY; CONFORMATION; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG BINDING; DRUG EFFECT; DRUG EFFICACY; DRUG INHIBITION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; MEMBRANE; MULTIDRUG RESISTANCE; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STIMULATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LUNG TUMOR; PATHOLOGY; TUMOR CELL LINE;

ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; NEOPLASM PROTEINS; ONCOGENE PROTEINS V-ERBB; PACLITAXEL; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, ERBB-2; THIAZOLES;

EID: 84902482999     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24787     Document Type: Article

References (50)

1. Allikmets R, Schriml LM, Hutchinson A, Romano-Spica V, Dean M. 1998. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 58:53375339.
2. Alqawi O, Bates S, Georges E. 2004. Arginine482 to threonine mutation in the breast cancer resistance protein ABCG2 inhibits rhodamine 123 transport while increasing binding. Biochem J 382:711716.
3. Ambudkar SV. 1998. Drug-stimulatable ATPase activity in crude membranes of human MDR1-transfected mammalian cells. Methods Enzymol 292: 504514.
4. Ambudkar SV, Cardarelli CO, Pashinsky I, Stein WD. 1997. Relation between the turnover number for vinblastine transport and for vinblastine-stimulated ATP hydrolysis by human P-glycoprotein. J Biol Chem 272:2116021166.
5. Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM. 2003. Pglycoprotein: From genomics to mechanism. Oncogene 22:74687485.
6. Anderson D. 2009. In vivo activity of ARRY-334543, a potent, small molecule inhibitor of EGFR/ErbB2 in combination with trastuzumab or docetaxel. AACR Meeting Abstracts 1757.
7. Cappuzzo F, Hirsch FR, Rossi E, Bartolini S, Ceresoli GL, Bemis L, Haney J, Witta S, Danenberg K, Domenichini I, Ludovini V, Magrini E, Gregorc V, Doglioni C, Sidoni A, Tonato M, Franklin WA, Crino L, Bunn PJ, Varella- Garcia M. 2005. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 97:643 655.
8. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. 1987. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 47:936942.
9. Chen YJ, Huang WC, Wei YL, Hsu SC, Yuan P, Lin HY, Wistuba II, Lee JJ, Yen CJ, Su WC, Chang KY, Chang WC, Chou TC, Chou CK, Tsai CH, Hung MC. 2011. Elevated BCRP/ABCG2 expression confers acquired resistance to gefitinib in wild-type EGFR-expressing cells. PLoS One 6:e21428.
10. Chen YN, Mickley LA, Schwartz AM, Acton EM, Hwang JL, Fojo AT. 1990. Characterization of adriamycin-resistant human breast cancer cells which display overexpression of a novel resistance-related membrane protein. J Biol Chem 265:1007310080.
11. Chen ZS, Hopper-Borge E, Belinsky MG, Shchaveleva I, Kotova E, Kruh GD. 2003. Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 63:351358.
12. Chen ZS, Tiwari AK. 2011. Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J 278:32263245.
13. Dai CL, Tiwari AK, Wu CP, Su XD, Wang SR, Liu DG, Ashby CJ, Huang Y, Robey RW, Liang YJ, Chen LM, Shi CJ, Ambudkar SV, Chen ZS, Fu LW. 2008. 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 68:79057914.
14. Dean M, Rzhetsky A, Allikmets R. 2001. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:11561166.
15. Doyle L, Ross DD. 2003. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 22:73407358.
16. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, Ross DD. 1998. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 95:1566515670.
17. Elkind NB, Szentpetery Z, Apati A, Ozvegy-Laczka C, Varady G, Ujhelly O, Szabo K, Homolya L, Varadi A, Buday L, Keri G, Nemet K, Sarkadi B. 2005. Multidrug transporter ABCG2 prevents tumor cell death induced by the epidermal growth factor receptor inhibitor Iressa (ZD1839, Gefitinib). Cancer Res 65:17701777.
18. Ellard S. 2009. ARRY-334543 in ErbB2 positive metastatic breast cancer and other ErbB expressing-cancers: Experience from expansion cohorts on a phase I study. AACR Meeting Abstracts 3603.
19. Goler-Baron V, Sladkevich I, Assaraf YG. 2012. Inhibition of the PI3K-Akt signaling pathway disrupts ABCG2-rich extracellular vesicles and overcomes multidrug resistance in breast cancer cells. Biochem Pharmacol 83:1340 1348.
20. Gottesman MM. 2002. Mechanisms of cancer drug resistance. Annu Rev Med 53:615627.
21. Gottesman MM, Fojo T, Bates SE. 2002. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer 2:4858.
22. Gottschling S, Schnabel PA, Herth FJ, Herpel E. 2012. Are we missing the target? Cancer stem cells and drug resistance in non-small cell lung cancer. Cancer Genomics Proteomics 9:275286.
23. Hazai E, Bikadi Z. 2008. Homology modeling of breast cancer resistance protein (ABCG2). J Struct Biol 162:6374.
24. Juliano RL, Ling V. 1976. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 455:152162.
25. Miknis G. 2005. ARRY-334543, A potent, orally active small molecule inhibitor of EGFR and ErbB-2. AACR Meeting Abstracts 801.
26. Miyake K, Mickley L, Litman T, Zhan Z, Robey R, Cristensen B, Brangi M, Greenberger L, Dean M, Fojo T, Bates SE. 1999. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 59:813.
27. Mogi M, Yang J, Lambert JF, Colvin GA, Shiojima I, Skurk C, Summer R, Fine A, Quesenberry PJ, Walsh K. 2003. Akt signaling regulates side population cell phenotype via Bcrp1 translocation. J Biol Chem 278:3906839075.
28. Nakanishi T, Ross DD. 2012. Breast cancer resistance protein (BCRP/ABCG2): Its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 31:7399.
29. Nakanishi T, Shiozawa K, Hassel BA, Ross DD. 2006. Complex interaction of BCRP/ABCG2 and imatinib in BCR-ABL-expressing cells: BCRP-mediated resistance to imatinib is attenuated by imatinib-induced reduction of BCRP expression. Blood 108:678684.
30. Nicolle E, Boumendjel A, Macalou S, Genoux E, Ahmed-Belkacem A, Carrupt PA, Di Pietro A. 2009. QSAR analysis and molecular modeling of ABCG2- specific inhibitors. Adv Drug Deliv Rev 61:3446.
31. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De Feo G, Caponigro F, Salomon DS. 2006. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366:216.
32. Pick A, Wiese M. 2012. Tyrosine kinase inhibitors influence ABCG2 expression in EGFR-positive MDCK BCRP cells via the PI3K/Akt signaling pathway. ChemMedChem 7:650662.
33. Pirker R, Pereira JR, von Pawel J, Krzakowski M, Ramlau R, Park K, de Marinis F, Eberhardt WE, Paz-Ares L, Storkel S, Schumacher KM, von Heydebreck A, Celik I, OByrne KJ. 2012. EGFR expression as a predictor of survival for firstline chemotherapy plus cetuximab in patients with advanced non-small-cell lung cancer: Analysis of data from the phase 3 FLEX study. Lancet Oncol 13:3342.
34. Robey RW, Honjo Y, Morisaki K, Nadjem TA, Runge S, Risbood M, Poruchynsky MS, Bates SE. 2003a. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 89:1971 1978.
35. Robey RW, Honjo Y, Morisaki K, Nadjem TA, Runge S, Risbood M, Poruchynsky MS, Bates SE. 2003b. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 89:19711978.
36. Robey RW, Honjo Y, van de Laar A, Miyake K, Regis JT, Litman T, Bates SE. 2001. A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim Biophys Acta 1512:171182.
37. Rosenberg MF, Bikadi Z, Chan J, Liu X, Ni Z, Cai X, Ford RC, Mao Q. 2010. The human breast cancer resistance protein (BCRP/ABCG2) shows conformational changes with mitoxantrone. Structure 18:482493.
38. Rusnak DW, Alligood KJ, Mullin RJ, Spehar GM, Arenas-Elliott C, Martin AM, Degenhardt Y, Rudolph SK, Haws TJ, Hudson-Curtis BL, Gilmer TM. 2007. Assessment of epidermal growth factor receptor (EGFR, ErbB1) and HER2 (ErbB2) protein expression levels and response to lapatinib (Tykerb, GW572016) in an expanded panel of human normal and tumour cell lines. Cell Prolif 40:580594.
39. Seshacharyulu P, Ponnusamy MP, Haridas D, Jain M, Ganti AK, Batra SK. 2012. Targeting the EGFR signaling pathway in cancer therapy. Expert Opin Ther Targets 16:1531.
40. Shi Z, Peng XX, Kim IW, Shukla S, Si QS, Robey RW, Bates SE, Shen T, Ashby CJ, Fu LW, Ambudkar SV, Chen ZS. 2007. 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 67:1101211020.
41. Shukla S, Chen ZS, Ambudkar SV. 2012. Tyrosine kinase inhibitors as modulators of ABC transporter-mediated drug resistance. Drug Resist Updat 15:7080.
42. Shukla S, Robey RW, Bates SE, Ambudkar SV. 2006. The calcium channel blockers, 1,4-dihydropyridines, are substrates of the multidrug resistancelinked ABC drug transporter, ABCG2. Biochemistry 45:89408951.
43. Sodani K, Patel A, Kathawala RJ, Chen ZS. 2012. Multidrug resistance associated proteins in multidrug resistance. Chin J Cancer 31:5872.
44. Sun YL, Chen JJ, Kumar P, Chen K, Sodani K, Patel A, Chen YL, Chen SD, Jiang WQ, Chen ZS. 2013. Reversal of MRP7 (ABCC10)-mediated multidrug resistance by tariquidar. PLoS One 8:e55576.
45. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:43504354.
46. Tsao MS, Sakurada A, Cutz JC, Zhu CQ, Kamel-Reid S, Squire J, Lorimer I, Zhang T, Liu N, Daneshmand M, Marrano P, Da CSG, Lagarde A, Richardson F, Seymour L, Whitehead M, Ding K, Pater J, Shepherd FA. 2005. Erlotinib in lung cancer molecular and clinical predictors of outcome. N Engl J Med 353:133144.
47. Yamazaki R, Nishiyama Y, Furuta T, Hatano H, Igarashi Y, Asakawa N, Kodaira H, Takahashi H, Aiyama R, Matsuzaki T, Yagi N, Sugimoto Y. 2011. Novel acrylonitrile derivatives, YHO-13177 and YHO-13351, reverse BCRP/ ABCG2-mediated drug resistance in vitro and in vivo. Mol Cancer Ther 10:12521263.
48. Yarden Y. 2001. The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur J Cancer 37(Suppl 4): S3S8.
49. Yoh K, Ishii G, Yokose T, Minegishi Y, Tsuta K, Goto K, Nishiwaki Y, Kodama T, Suga M, Ochiai A. 2004. Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 10:16911697.
50. Zhou S, Morris JJ, Barnes Y, Lan L, Schuetz JD, Sorrentino BP. 2002. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci USA 99:1233912344.