Identification of new MRP4 inhibitors from a library of FDA approved drugs using a high-throughput bioluminescence screen

Biochemical Pharmacology

Volumn 93, Issue 3, 2015, Pages 380-388

  Cheung, Leanna ^a   Yu, Denise M T ^a   Neiron, Zillan ^a   Failes, Tim W ^a   Arndt, Greg M ^a   Fletcher, Jamie I ^a  

^a University of New South Wales Sydney   (Australia)

Author keywords

ABCC4; Bioluminescence; High throughput screening; MRP4 inhibitor; Multidrug resistance

Indexed keywords

4 (3 BROMOANILINO) 6 (METHYLAMINO)PYRIDO[3,4 D]PYRIMIDINE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 4 (3 CHLOROPHENYL) 1,7 DIETHYLPYRIDO[2,3 D]PYRIMIDIN 2(1H) ONE; 4 AMINO 5 (3 BROMOPHENYL) 7 (6 MORPHOLINO 3 PYRIDINYL)PYRIDO[2,3 D]PYRIMIDINE; 5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; 9 CHLORO 2 (2 FURYL) 5,6 DIHYDRO 5 IMINO 1,2,4 TRIAZOLO[2,3 C]QUINAZOLINE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CEEFOURIN 1; CILOSTAMIDE; CILOSTAZOL; DANTROLENE; ERLOTINIB; EUPATORIN; FIRTECAN; GEFITINIB; GLAFENINE; GW 2974; KI 8751; MERCAPTOPURINE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4 INHIBITOR; NALIDIXIC ACID; PHOSPHODIESTERASE INHIBITOR; PRAZOSIN; PROTEIN INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; PSB 36; SB 408124; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERLUKAST; ZM 306416; ABCC4 PROTEIN, HUMAN; CAMPTOTHECIN; IRINOTECAN; LUCIFERASE; MOLECULAR LIBRARY; MULTIDRUG RESISTANCE PROTEIN;

ARTICLE; BIOLUMINESCENCE; CELL LINE; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG SENSITIZATION; FEMALE; FOOD AND DRUG ADMINISTRATION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANALYSIS; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG APPROVAL; HEK293 CELL LINE; LUMINESCENCE; METABOLISM; MOLECULAR LIBRARY; PHARMACOLOGY; PROCEDURES; UNITED STATES;

6-MERCAPTOPURINE; CAMPTOTHECIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG APPROVAL; HEK293 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; SMALL MOLECULE LIBRARIES; UNITED STATES;

EID: 84921813458     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.11.006     Document Type: Article

References (37)

1. Schuetz JD, Connelly MC, Sun D, Paibir SG, Flynn PM, Srinivas RV, et al. MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat Med 1999;5:1048-51.
2. Russel FG, Koenderink JB, Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 2008;29:200-7.
3. Belinsky MG, Guo P, Lee K, Zhou F, Kotova E, Grinberg A, et al. Multidrug resistance protein 4 protects bone marrow, thymus, spleen, and intestine from nucleotide analogue-induced damage. Cancer Res 2007;67:262-8.
4. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, et al. Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 2004;24:7612-21.
5. Henderson MJ, Haber M, Porro A, Munoz MA, Iraci N, Xue C, et al. ABCC multidrug transporters in childhood neuroblastoma: clinical and biological effects independent of cytotoxic drug efflux. J Natl Cancer Inst 2011;103:1236-51.
6. Norris MD, Smith J, Tanabe K, Tobin P, Flemming C, Scheffer GL, 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;4:547-53.
7. Holla VR, Backlund MG, Yang P, Newman RA, DuBois RN. Regulation of prostaglandin transporters in colorectal neoplasia. Cancer Prev Res (Phila Pa) 2008;1:93-9.
8. Heimerl S, Bosserhoff AK, Langmann T, Ecker J, Schmitz G. Mapping ATPbinding cassette transporter gene expression profiles in melanocytes and melanoma cells. Melanoma Res 2007;17:265-73.
9. Cai C, Omwancha J, Hsieh CL, Shemshedini L. Androgen induces expression of the multidrug resistance protein gene MRP4 in prostate cancer cells. Prostate Cancer Prostatic Dis 2007;10:39-45.
10. Copsel S, Garcia C, Diez F, Vermeulem M, Baldi A, Bianciotti LG, et al. Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation. J Biol Chem 2011;286:6979-88.
11. Haimeur A, Conseil G, Deeley RG, Cole SP. The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr Drug Metab 2004;5:21-53.
12. Xie M, Rich TC, Scheitrum C, Conti M, Richter W. Inactivation of multidrug resistance proteins disrupts both cellular extrusion and intracellular degradation of cAMP. Mol Pharmacol 2011;80:281-93.
13. Cheung L, Flemming CL, Watt F, Masada N, Yu DM, Huynh T, et al. High-throughput screening identifies Ceefourin 1 and Ceefourin 2 as highly selective inhibitors of multidrug resistance protein 4 (MRP4). Biochem Pharmacol 2014;91:97-108.
14. Zhang Y, Bressler JP, Neal J, Lal B, Bhang HE, Laterra J, et al. ABCG2/BCRP expression modulates D -luciferin based bioluminescence imaging. Cancer Res 2007;67:9389-97.
15. Wielinga PR, Reid G, Challa EE, van der Heijden I, van Deemter L, de Haas M, et al. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharmacol 2002;62:1321-31.
16. Kinsella TM, Nolan GP. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 1996;7:1405-13.
17. Ponomarev V, Doubrovin M, Serganova I, Vider J, Shavrin A, Beresten T, et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent,and nuclear noninvasive imaging. Eur J Nucl Med Mol Imaging 2004;31:740-51.
18. Loe DW, Almquist KC, Deeley RG, Cole SP. Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 1996;271:9675-82.
19. Myette RL, Conseil G, Ebert SP, Wetzel B, Detty MR, Cole SP. Chalcogenopyrylium dyes as differential modulators of organic anion transport by multidrug resistance protein 1 (MRP1), MRP2, and MRP4. Drug Metab Dispos 2013;41:1231-9.
20. Zhang JH, Chung TD, Oldenburg KR. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999;4:67-73.
21. Chen ZS, Lee K, Walther S, Raftogianis RB, Kuwano M, Zeng H, et al. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 2002;62:3144-50.
22. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, et al. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 2003;100:9244-9.
23. Lembert N, Idahl LA. Regulatory effects of ATP and luciferin on firefly luciferase activity. Biochem J 1995;305(Pt 3):929-33.
24. Chen ZS, Lee K, Kruh GD. 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;276:33747-54.
25. Zhang Y, Byun Y, Ren YR, Liu JO, Laterra J, Pomper MG. Identification of inhibitors of ABCG2 by a bioluminescence imaging-based high-throughput assay. Cancer Res 2009;69:5867-75.
26. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, et al. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 2003;63:1094-103.
27. Wu CP, Calcagno AM, Hladky SB, Ambudkar SV, Barrand MA. Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J 2005;272:4725-40.
28. Shi Z, Tiwari AK, Shukla S, Robey RW, Kim IW, Parmar S, et al. Inhibiting the function of ABCB1 and ABCG2 by the EGFR tyrosine kinase inhibitor AG1478. Biochem Pharmacol 2009;77:781-93.
29. Rabindran SK, Ross DD, Doyle LA, Yang W, Greenberger LM. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res 2000;60:47-50.
30. Tian Q, Zhang J, Tan TM, Chan E, Duan W, Chan SY, et al. Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm Res 2005;22:1837-53.
31. Yang CJ, Horton JK, Cowan KH, Schneider E. Cross-resistance to camptothecin analogues in a mitoxantrone-resistant human breast carcinoma cell line is not due to DNA topoisomerase I alterations. Cancer Res 1995;55:4004-9.
32. Mattiello T, Guerriero R, Lotti LV, Trifiro E, Felli MP, Barbarulo A, et al. Aspirin extrusion from human platelets through multidrug resistance protein-4-mediated transport: evidence of a reduced drug action in patients after coronary artery bypass grafting. J Am Coll Cardiol 2011;58:752-61.
33. Hara Y, Sassi Y, Guibert C, Gambaryan N, Dorfmuller P, Eddahibi S, et al. Inhibition of MRP4 prevents and reverses pulmonary hypertension in mice. J Clin Invest 2011;121:2888-97.
34. Fukuda Y, Takenaka K, Sparreboom A, Cheepala SB, Wu CP, Ekins S, et al. Human immunodeficiency virus protease inhibitors interact with ABCC4/ MRP4: a basis for unanticipated enhanced cytotoxicity. Mol Pharmacol 2013.
35. Auld DS, Southall NT, Jadhav A, Johnson RL, Diller DJ, Simeonov A, et al. Characterization of chemical libraries for luciferase inhibitory activity. J Med Chem 2008;51:2372-86.
36. US Food Drug Administration Center for Drug Evaluation and Research. Approved Drug Products with Therapeutic Equivalence Evaluations. 34th Edition, US Department of Health and Human Services; 2014.
37. Berger F, Paulmurugan R, Bhaumik S, Gambhir SS. Uptake kinetics and biodistribution of 14C-D-luciferin - a radiolabeled substrate for the firefly luciferase catalyzed bioluminescence reaction: impact on bioluminescence based reporter gene imaging. Eur J Nucl Med Mol Imaging 2008;35:2275-85.