Mouse ATP-binding cassette (ABC) transporters conferring multi-drug resistance

Anti-Cancer Agents in Medicinal Chemistry

Volumn 15, Issue 4, 2015, Pages 423-432

  Li, Shuaizhang ^a   Zhang, Wen ^b   Yin, Xuejiao ^a   Xing, Shilai ^c   Xie, Heidi Qunhui ^a   Cao, Zhengyu ^d   Zhao, Bin ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b NANJING INSTITUTE OF ENVIRONMENTAL SCIENCES   (China)

^c INSTITUTE OF BOTANY   (China)

^d CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

ATP binding cassette (ABC) transporter; Cancer; Inhibitors; Multi drug resistance; Substrate

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; CRK ASSOCIATED SUBSTRATE PROTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; ABCG2 PROTEIN, MOUSE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 1;

ARTICLE; CANCER CHEMOTHERAPY; DRUG ACTIVITY; ENZYME ACTIVITY; HUMAN; MULTIDRUG RESISTANCE; NEOPLASM; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; DRUG RESISTANCE; GENETICS; METABOLISM; MOUSE; NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASMS; P-GLYCOPROTEIN;

EID: 84929674053     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/1871520615666150129212723     Document Type: Article

References (127)

1. Higgins, C.F. ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol., 1992, 8, 67-113.
2. Dean, M.; Rzhetsky, A.; Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res., 2001, 11 (7), 1156-1166.
3. 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 (6282), 362-365.
4. Schmitt, L.; Tampe, R. Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol., 2002, 12 (6), 754-760.
5. Zolnerciks, J. K.; Akkaya, B. G.; Snippe, M.; Chiba, P.; Seelig, A.; Linton, K.J. The Q loops of the human multidrug resistance transporter ABCB1 are necessary to couple drug binding to the ATP catalytic cycle. FASEB J., 2014, 28 (10), 4335-4346.
6. Francone, O.L.; Subbaiah, P.V.; Van Tol, A.; Royer, L.; Haghpassand, M. Abnormal phospholipid composition impairs HDL biogenesis and maturation in mice lacking Abca1. Biochemistry, 2003, 42 (28), 8569-8578.
7. Mack, J.T.; Beljanski, V.; Soulika, A.M.; Townsend, D.M.; Brown, C.B.; Davis, W.; Tew, K.D. "Skittish" Abca2 knockout mice display tremor, hyperactivity, and abnormal myelin ultrastructure in the central nervous system. Mol. Cell. Biol., 2007, 27 (1), 44-53.
8. Ban, N.; Matsumura, Y.; Sakai, H.; Takanezawa, Y.; Sasaki, M.; Arai, H.; Inagaki, N. ABCA3 as a lipid transporter in pulmonary surfactant biogenesis. J. Biol. Chem., 2007, 282 (13), 9628-9634.
9. Weng, J.; Mata, N. L.; Azarian, S.M.; Tzekov, R.T.; Birch, D. G.; Travis, G. H. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell, 1999, 98 (1), 13-23.
10. Kim, W.S.; Fitzgerald, M.L.; Kang, K.W.; Okuhira, K.; Bell, S.A.; Manning, J.J.; Koehn, S. L.; Lu, N. F.; Moore, K.J.; Freeman, M.W. Abca7 null mice retain normal macrophage phosphatidyleholine and cholesterol efflux activity despite alterations in adipose mass and serum cholesterol levels. J. Biol. Chem., 2005, 280 (5), 3989-3995.
11. Volm, M.; Efferth, T.; Mattern, J.; Pommerenke, E. W. Resistance Mechanisms in Murine Tumors with Acquired Multidrug Resistance. ARZNEIMITTEL-FORSCH., 1992, 42-2 (9), 1163-1168.
12. Li, F. Q.; Guo, J.; Fu, Y. N.; Yan, G.; Faustman, D. Abnormal Class-I Assembly and Peptide Presentation in the Nonobese Diabetic Mouse. Proc. Natl. Acad. Sci. U S A., 1994, 91 (23), 11128-11132.
13. Brown, M. G.; Driscoll, J.; Monaco, J. J. Structural and Serological Similarity of Mhc-Linked Lmp and Proteasome (Multicatalytic Proteinase) Complexes. Nature, 1991, 353 (6342), 355-357.
14. Fickert, P.; Wagner, M.; Marschall, H. U.; Fuchsbichler, A.; Zollner, G.; Tsybrovskyy, O.; Zatloukal, K.; Liu, J.; Waalkes, M. P.; Cover, C.; Denk, H.; Hofman, A. F.; Jaeschke, H.; Trauner, M. 24-norUrsodeoxycholic acid is superior to ursodeoxycholic acid in the treatment of sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology, 2006, 130 (2), 465-481.
15. Krishnamurthy, P.C.; Du, G. Q.; Fukuda, Y.; Sun, D. X.; Sampath, J.; Mercer, K. E.; Wang, J. F.; Sosa-Pineda, B.; Murti, K. G.; Schuetz, J.D. Identification of a mammalian mitochondrial porphyrin transporter. Nature, 2006, 443 (7111), 586-589.
16. Pondarre, C.; Antiochos, B. B.; Campagna, D. R.; Greer, E. L.; Deck, K.M.; McDonald, A.; Han, A. P.; Medlock, A.; Kutok, J.L.; Anderson, S.A.; Eisenstein, R.S.; Fleming, M.D. The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis. Hum. Mol. Gene., 2006, 15 (6), 953-964.
17. Shirihai, O. S.; Gregory, T.; Yu, C.N.; Orkin, S.H.; Weiss, M.J. ABC-me: A novel mitochondrial transporter induced by GATA-1 during erythroid differentiation. Embo. J., 2000, 19 (11), 2492-2502.
18. Wang, R.X.; Salem, M.; Yousef, I.M.; Tuchweber, B.; Lam, P.; Childs, S.J.; Helgason, C.D.; Ackerley, C.; Phillips, M.J.; Ling, V. Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis. Proc. Natl. Acad. Sci. U S A., 2001, 98 (4), 2011-2016.
19. Nielsen, D.; Maare, C.; Eriksen, J.; Litman, T.; Skovsgaard, T. Expression of P-glycoprotein associated protein in Ehrlich fractionated and multidrug resistance ascites tumor cells after irradiation. Int. J. Radiat. Oncol., 2001, 51 (4), 1050-1057.
20. Vlaming, M.L.; Mohrmann, K.; Wagenaar, E.; de Waart, D.R.; Elferink, R.P.; Lagas, J.S.; Van Tellingen, O.; Vainchtein, L.D.; Rosing, H.; Beijnen, J.H.; Schellens, J.H.; Schinkel, A.H. Carcinogen and anticancer drug transport by Mrp2 in vivo: Studies using Mrp2 (Abcc2) knockout mice. J. Pharmacol. Exp. Ther., 2006, 318 (1), 319-327.
21. Zamek-Gliszczynski, M.J.; Nezasa, K.; Tian, X.; Bridges, A. S.; Lee, K.; Belinsky, M.G.; Kruh, G.D.; Brouwer, K.L. Evaluation of the role of multidrug resistance-associated protein (Mrp) 3 and Mrp4 in hepatic basolateral excretion of sulfate and glucuronide metabolites of acetaminophen, 4-methylumbelliferone, and harmol in Abcc3-/-and Abcc4-/-mice. J. Pharmacol. Exp. Ther., 2006, 319 (3), 1485-1491.
22. Denk, G.U.; Soroka, C.J.; Takeyama, Y.; Chen, W.S.; Schuetz, J. D.; Boyer, J.L. Multidrug resistance-associated protein 4 is upregulated in liver but down-regulated in kidney in obstructive cholestasis in the rat. J. Hepatol., 2004, 40 (4), 585-591.
23. Lee, Y.J.; Kusuhara, H.; Sugiyama, Y. Do multidrug resistanceassociated protein-1 and-2 play any role in the elimination of estradiol-17 beta-glucuronide and 2,4-dinitrophenyl-S-glutathione across the blood-cerebrospinal fluid barrier? J. Pharm. Sci., 2004, 93 (1), 99-107.
24. Gorgels, T.G. M.F.; Hu, X.F.; Scheffer, G. L.; Van der Wal, A.C.; Toonstra, J.; De Jong, P.T.V. M.; Van Kuppevelt, T.H.; Levelt, C. N.; De Wolf, A.; Loves, W.J.P.; Scheper, R.J.; Peek, R.; Bergen, A. A.B. Disruption of Abcc6 in the mouse: Novel insight in the pathogenesis of pseudoxanthoma elasticum. Hum. Mol. Gene., 2005, 14 (13), 1763-1773.
25. Chen, H.; Ruan, Y.C.; Xu, W. M.; Chen, J.; Chan, H.C. Regulation of male fertility by CFTR and implications in male infertility. Hum. Reprod. Update, 2012, 18 (6), 703-713.
26. Seghers, V.; Nakazaki, M.; DeMayo, F.; Aguilar-Bryan, L.; Bryan, J. Sur1 knockout mice-A model for K-ATP channel-independent regulation of insulin secretion. J. Biol. Chem., 2000, 275(13), 9270-9277.
27. Chutkow, W.A.; Samuel, V.; Hansen, P.A.; Pu, J.L.; Valdivia, C. R.; Makielski, J.C.; Burant, C.F. Disruption of Sur2-containing KATP channels enhances insulin-stimulated glucose uptake in skeletal muscle. Proc. Natl. Acad. Sci. U S A., 2001, 98 (20), 11760-11764.
28. Fouquet, F.; Zhou, J.M.; Ralston, E.; Murray, K.; Troalen, F.; Magal, E.; Robain, O.; Dubois-Dalcq, M.; Aubourg, P. Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol Dis., 1997, 3(4), 271-285.
29. Bisbal, C.; Silhol, M.; Laubenthal, K.; Kaluza, T.; Carnac, G.; Milligan, L.; Le Roy, F.; Salehzada, T. The 2 '-5 ' oligoadenylate/ RNase L/RNase L inhibitor pathway regulates both MyoD mRNA stability and muscle cell differentiation. Mol. Cell. Biol., 2000, 20 (14), 4959-4969.
30. Nakamura, K.; Kennedy, M. A.; Baldan, A.; Bojanic, D. D.; Lyons, K.; Edwards, P.A. Expression and regulation of multiple murine ATP-binding cassette transporter G1 mRNAs/isoforms that stimulate cellular cholesterol efflux to high density lipoprotein. J. Biol. Chem., 2004, 279 (44), 45980-45989.
31. Allen, J. D.; Jackson, S. C.; Schinkel, A. H. A mutation hot spot in the Bcrp1 (Abcg2) multidrug transporter in mouse cell lines selected for Doxorubicin resistance. Cancer Res., 2002, 62(8), 2294-2299.
32. Plosch, T.; Van der Veen, J.N.; Havinga, R.; Huijkman, N.C.; Bloks, V. W.; Kuipers, F. Abcg5/Abcg8-independent pathways contribute to hepatobiliary cholesterol secretion in mice. Am. J. Physiol-gastr. L., 2006, 291 (3), G414-423.
33. Simon, S.M.; Schindler, M. Cell biological mechanisms of multidrug resistance in tumors. Proc Proc. Natl. Acad. Sci. U S A., 1994, 91 (9), 3497-3504.
34. Domanitskaya, N.; Wangari-Talbot, J.; Jacobs, J.; Peiffer, E.; Mahdaviyeh, Y.; Paulose, C.; Malofeeva, E.; Foster, K.; Cai, K.Q.; Zhou, Y.; Egleston, B.; Hopper-Borge, E. Abcc10 status affects mammary tumour growth, metastasis, and docetaxel treatment response. Brit. J. Cancer., 2014, 111(4), 696-707.
35. Fletcher, J.I.; Haber, M.; Henderson, M.J.; Norris, M.D. ABC transporters in cancer: More than just drug efflux pumps. Nat. Rev. Cancer., 2010, 10 (2), 147-156.
36. Costa, J.; Reis-Henriques, M.A.; Castro, L.F.; Ferreira, M. Gene expression analysis of ABC efflux transporters, CYP1A and GSTalpha in Nile tilapia after exposure to benzo(a)pyrene. Comp. Biochem. Phys. C, 2012, 155(3), 469-482.
37. Ambudkar, S.V.; Dey, S.; Hrycyna, C.A.; Ramachandra, M.; Pastan, I.; Gottesman, M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol.Toxicol., 1999, 39, 361-398.
38. Gottesman, M.M.; Fojo, T.; Bates, S. E. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer, 2002, 2(1), 48-58.
39. Shepard, R. L.; Cao, J.; Starling, J. J.; Dantzig, A. H. Modulation of P-glycoprotein but not MRP1-or BCRP-mediated drug resistance by LY335979. Int. J. Cancer., 2003, 103 (1), 121-125.
40. Chen, C.J.; Chin, J.E.; Ueda, K.; Clark, D.P.; Pastan, I.; Gottesman, M.M.; Roninson, I.B. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell, 1986, 47 (3), 381-389.
41. Ueda, K.; Pastan, I.; Gottesman, M.M. Isolation and sequence of the promoter region of the human multidrug-resistance (P-glycoprotein) gene. J. Biol. Chem., 1987, 262 (36), 17432-17436.
42. Cole, S.P.; Bhardwaj, G.; Gerlach, J.H.; Mackie, J. E.; Grant, C.E.; Almquist, K.C.; Stewart, A.J.; Kurz, E.U.; Duncan, A.M.; Deeley, R. G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 1992, 258 (5088), 1650-1654.
43. 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. U S A., 1998, 95 (26), 15665-15670.
44. Allikmets, R.; Schriml, L.M.; Hutchinson, A.; Romano-Spica, V.; Dean, M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res., 1998, 58 (23), 5337-5339.
45. Allikmets, R.; Wasserman, W. W.; Hutchinson, A.; Smallwood, P.; Nathans, J.; Rogan, P.K.; Schneider, T.D.; Dean, M. Organization of the ABCR gene: Analysis of promoter and splice junction sequences. Gene, 1998, 215 (1), 111-122.
46. Lagas, J.S.; Vlaming, M.L.; Schinkel, A.H. Pharmacokinetic assessment of multiple ATP-binding cassette transporters: The power of combination knockout mice. Mol. Interv., 2009, 9 (3), 136-145.
47. Schumacher, T.; Krohn, M.; Hofrichter, J.; Lange, C.; Stenzel, J.; Steffen, J.; Dunkelmann, T.; Paarmann, K.; Frohlich, C.; Uecker, A.; Plath, A. S.; Sommer, A.; Bruning, T.; Heinze, H. J.; Pahnke, J. ABC transporters B1, C1 and G2 differentially regulate neuroregeneration in mice. PLoS One., 2012, 7 (4), e35613.
48. Li, L.; Shukla, S.; Lee, A.; Garfield, S.H.; Maloney, D.J.; Ambudkar, S.V.; Yuspa, S. H. The skin cancer chemotherapeutic agent ingenol-3-angelate (PEP005) is a substrate for the epidermal multidrug transporter (ABCB1) and targets tumor vasculature. Cancer Res., 2010, 70 (11), 4509-4519.
49. 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 (1), 3-29.
50. Borst, P.; Schinkel, A. H. P-glycoprotein ABCB1: a major player in drug handling by mammals. J. Clin. Invest., 2013, 123 (10), 4131-4133.
51. Boesch, D.; Gaveriaux, C.; Jachez, B.; Pourtier-Manzanedo, A.; Bollinger, P.; Loor, F. In vivo circumvention of P-glycoproteinmediated multidrug resistance of tumor cells with SDZ PSC 833. Cancer Res., 1991, 51 (16), 4226-4233.
52. Dantzig, A.H.; Shepard, R.L.; Cao, J.; Law, K.L.; Ehlhardt, W.J.; Baughman, T.M.; Bumol, T.F.; Starling, J.J. Reversal of Pglycoprotein-mediated multidrug resistance by a potent cyclopropyldibenzosuberane modulator, LY335979. Cancer Res., 1996, 56 (18), 4171-4179.
53. Allen, J.D.; Brinkhuis, R.F.; Van Deemter, L.; Wijnholds, J.; Schinkel, A.H. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res., 2000, 60 (20), 5761-5766.
54. Allen, J.D.; Van Dort, S.C.; Buitelaar, M.; Van Tellingen, O.; Schinkel, A.H. Mouse breast cancer resistance protein (Bcrp1/Abcg2) mediates etoposide resistance and transport, but etoposide oral availability is limited primarily by P-glycoprotein. Cancer Res., 2003, 63 (6), 1339-1344.
55. Lorico, A.; Rappa, G.; Finch, R.A.; Yang, D.; Flavell, R.A.; Sartorelli, A.C. Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res., 1997, 57 (23), 5238-5242.
56. Cisternino, S.; Rousselle, C.; Lorico, A.; Rappa, G.; Scherrmann, J.M. Apparent lack of Mrp1-mediated efflux at the luminal side of mouse blood-brain barrier endothelial cells. Pharm. Res., 2003, 20 (6), 904-909.
57. Echevarria-Lima, J.; Kyle-Cezar, F.; DF, P.L.; Capella, L.; Capella, M.A.; Rumjanek, V. M. Expression and activity of multidrug resistance protein 1 in a murine thymoma cell line. Immunology, 2005, 114 (4), 468-475.
58. Zander, S.A.; Kersbergen, A.; Van der Burg, E.; De Water, N.; Van Tellingen, O.; Gunnarsdottir, S.; Jaspers, J.E.; Pajic, M.; Nygren, A.O.; Jonkers, J.; Borst, P.; Rottenberg, S. Sensitivity and acquired resistance of BRCA1;p53-deficient mouse mammary tumors to the topoisomerase I inhibitor topotecan. Cancer Res., 2010, 70(4), 1700-1710.
59. Allen, J.D.; Brinkhuis, R.F.; Wijnholds, J.; Schinkel, A. H. The mouse Bcrp1/Mxr/Abcp gene: Amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res., 1999, 59 (17), 4237-4241.
60. Robey, R.W.; Steadman, K.; Polgar, O.; Morisaki, K.; Blayney, M.; Mistry, P.; Bates, S.E. Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res., 2004, 64 (4), 1242-1246.
61. Allen, J.D.; van Loevezijn, A.; Lakhai, J.M.; Van der Valk, M.; Van Tellingen, O.; Reid, G.; Schellens, J.H.; Koomen, G.J.; Schinkel, A. H. Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer. Ther., 2002, 1 (6), 417-425.
62. Zhou, L.; Schmidt, K.; Nelson, F.R.; Zelesky, V.; Troutman, M.D.; Feng, B. The effect of breast cancer resistance protein and Pglycoprotein on the brain penetration of flavopiridol, imatinib mesylate (Gleevec), prazosin, and 2-methoxy-3-(4-(2-(5-methyl-2-phenyloxazol-4-yl) ethoxy) pheny l) propanoic acid (PF-407288) in mice. Drug. Metab. Dispos., 2009, 37 (5), 946-955.
63. Shukla, S.; Zaher, H.; Hartz, A.; Bauer, B.; Ware, J. A.; Ambudkar, S. V. Curcumin inhibits the activity of ABCG2/BCRP1, a multidrug resistance-linked ABC drug transporter in mice. Pharm. Res., 2009, 26 (2), 480-487.
64. Bakhsheshian, J.; Hall, M. D.; Robey, R.W.; Herrmann, M.A.; Chen, J.Q.; Bates, S.E.; Gottesman, M. M. Overlapping substrate and inhibitor specificity of human and murine ABCG2. Drug. Metab. Dispos., 2013, 41 (10), 1805-1812.
65. Erlichman, C.; Boerner, S. A.; Hallgren, C. G.; Spieker, R.; Wang, X.Y.; James, C.D.; Scheffer, G.L.; Maliepaard, M.; Ross, D.D.; Bible, K.C.; Kaufmann, S. H. The HER tyrosine kinase inhibitor CI1033 enhances cytotoxicity of 7-ethyl-10-hydroxycamptothecin and topotecan by inhibiting breast cancer resistance proteinmediated drug efflux. Cancer Res., 2001, 61 (2), 739-748.
66. Stewart, C. F.; Leggas, M.; Schuetz, J. D.; Panetta, J. C.; Cheshire, P. J.; Peterson, J.; Daw, N.; Jenkins, J. J., 3rd; Gilbertson, R.; Germain, G. S.; Harwood, F. C.; Houghton, P. J. Gefitinib enhances the antitumor activity and oral bioavailability of irinotecan in mice. Cancer Res., 2004, 64 (20), 7491-7499.
67. 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 (1), 52-61.
68. Yamazaki, R.; Nishiyama, Y.; Furuta, T.; Hatano, H.; Igarashi, Y.; Asakawa, N.; Kodaira, H.; Takahashi, H.; Aiyama, R.; Matsuzaki, T.; Yagi, N.; Sugimoto, Y. Novel acrylonitrile derivatives, YHO-13177 and YHO-13351, reverse BCRP/ABCG2-mediated drug resistance in vitro and in vivo. Mol. Cancer. Ther., 2011, 10 (7), 1252-1263.
69. Mazard, T.; Causse, A.; Simony, J.; Leconet, W.; Vezzio-Vie, N.; Torro, A.; Jarlier, M.; Evrard, A.; Del Rio, M.; Assenat, E.; Martineau, P.; Ychou, M.; Robert, B.; Gongora, C. Sorafenib overcomes irinotecan resistance in colorectal cancer by inhibiting the ABCG2 drug-efflux pump. Mol. Cancer. Ther., 2013, 12 (10), 2121-2134.
70. Devault, A.; Gros, P. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol. Cell. Biol., 1990, 10 (4), 1652-1663.
71. Silverman, M. Structure and function of hexose transporters. Annu. Rev. Biochem., 1991, 60, 757-794.
72. Schinkel, A. H. The physiological function of drug-transporting Pglycoproteins. Semin. Cancer. Biol., 1997, 8 (3), 161-170.
73. Sikic, B.I. Pharmacologic approaches to reversing multidrug resistance. Semin. Hematol., 1997, 34 (4 Suppl 5), 40-47.
74. Schinkel, A.H.; Smit, J.J.; van Tellingen, O.; Beijnen, J.H.; Wagenaar, E.; van Deemter, L.; Mol, C.A.; Van der Valk, M.A.; Robanus-Maandag, E.C.; te Riele, H.P. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell, 1994, 77 (4), 491-502.
75. 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 (7-8), 1295-1298.
76. Borst, P. Cancer drug pan-resistance: Pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open. Biol., 2012, 2 (5), 120066.
77. Thomas, H.; Coley, H.M. Overcoming multidrug resistance in cancer: An update on the clinical strategy of inhibiting pglycoprotein. Cancer Control, 2003, 10 (2), 159-165.
78. Schinkel, A.H.; Jonker, J.W. Polymorphisms affecting function of the human organic cation transporter hOCT1 (SLC22A1): What are the consequences? Pharmacogenetics, 2002, 12(8), 589-590.
79. Hyafil, F.; Vergely, C.; Du Vignaud, P.; Grand-Perret, T. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res., 1993, 53 (19), 4595-4602.
80. Malingre, M.M.; Beijnen, J.H.; Rosing, H.; Koopman, F. J.; Jewell, R.C.; Paul, E.M.; Ten Bokkel Huinink, W.W.; Schellens, J.H. Coadministration of GF120918 significantly increases the systemic exposure to oral paclitaxel in cancer patients. Brit. J. Cancer., 2001, 84 (1), 42-47.
81. Dantzig, A.H.; Law, K.L.; Cao, J.; Starling, J.J. Reversal of multidrug resistance by the P-glycoprotein modulator, LY335979, from the bench to the clinic. Curr. Med. Chem., 2001, 8 (1), 39-50.
82. Mistry, P.; Stewart, A. J.; Dangerfield, W.; Okiji, S.; Liddle, C.; Bootle, D.; Plumb, J. A.; Templeton, D.; Charlton, P. In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Res., 2001, 61 (2), 749-758.
83. Newman, M. J.; Rodarte, J. C.; Benbatoul, K. D.; Romano, S. J.; Zhang, C.; Krane, S.; Moran, E.J.; Uyeda, R.T.; Dixon, R.; Guns, E.S.; Mayer, L.D. Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance. Cancer Res., 2000, 60 (11), 2964-2972.
84. Tang, S. J.; Chen, L.K.; Wang, F.; Zhang, Y.K.; Huang, Z.C.; To, K.K.; Wang, X. K.; Talele, T.T.; Chen, Z.S.; Chen, W.Q.; Fu, L. W. CEP-33779 antagonizes ATP-binding cassette subfamily B member 1 mediated multidrug resistance by inhibiting its transport function. Biochem. Pharmacol., 2014, 91 (2), 144-156.
85. Pichler, A.; Zelcer, N.; Prior, J. L.; Kuil, A. J.; Piwnica-Worms, D. In vivo RNA interference-mediated ablation of MDR1 Pglycoprotein. Clin. Cancer. Res., 2005, 11 (12), 4487-4494.
86. Yague, E.; Higgins, C. F.; Raguz, S. Complete reversal of multidrug resistance by stable expression of small interfering RNAs targeting MDR1. Gene Ther., 2004, 11 (14), 1170-1174.
87. Patil, Y.B.; Swaminathan, S.K.; Sadhukha, T.; Ma, L.; Panyam, J. The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials, 2010, 31 (2), 358-365.
88. Lin, G.; Zhu, W.; Yang, L.; Wu, J.; Lin, B.; Xu, Y.; Cheng, Z.; Xia, C.; Gong, Q.; Song, B.; Ai, H. Delivery of siRNA by MRI-visible nanovehicles to overcome drug resistance in MCF-7/ADR human breast cancer cells. Biomaterials, 2014, 35 (35), 9495-9507.
89. Shen, J.; Wang, Q.; Hu, Q.; Li, Y.; Tang, G.; Chu, P.K. Restoration of chemosensitivity by multifunctional micelles mediated by P-gp siRNA to reverse MDR. Biomaterials, 2014, 35 (30), 8621-8634.
90. Eyre, R.; Harvey, I.; Stemke-Hale, K.; Lennard, T.W.; Tyson-Capper, A.; Meeson, A.P. Reversing paclitaxel resistance in ovarian cancer cells via inhibition of the ABCB1 expressing side population. Tumour Biol., 2014, 35 (10), 9879-9892.
91. Stride, B.D.; Valdimarsson, G.; Gerlach, J.H.; Wilson, G. M.; Cole, S.P.; Deeley, R.G. Structure and expression of the messenger RNA encoding the murine multidrug resistance protein, an ATP-binding cassette transporter. Mol. Pharmacol., 1996, 49 (6), 962-971.
92. Leslie, E. M.; Deeley, R. G.; Cole, S. P. Multidrug resistance proteins: Role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol., 2005, 204 (3), 216-237.
93. Ito, K.; Olsen, S.L.; Qiu, W.; Deeley, R.G.; Cole, S.P. Mutation of a single conserved tryptophan in multidrug resistance protein 1 (MRP1/ABCC1) results in loss of drug resistance and selective loss of organic anion transport. J. Biol. Chem., 2001, 276 (19), 15616-15624.
94. Haimeur, A.; Conseil, G.; Deeley, R. G.; Cole, S. P. The MRPrelated and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr. Drug. Metab., 2004, 5 (1), 21-53.
95. Zhang, D.W.; Cole, S.P.; Deeley, R.G. Identification of a nonconserved amino acid residue in multidrug resistance protein 1 important for determining substrate specificity: evidence for functional interaction between transmembrane helices 14 and 17. J. Biol. Chem., 2001, 276 (37), 34966-34974.
96. Campbell, J. D.; Deol, S. S.; Ashcroft, F. M.; Kerr, I. D.; Sansom, M. S. Nucleotide-dependent conformational changes in HisP: molecular dynamics simulations of an ABC transporter nucleotidebinding domain. Biophys. J., 2004, 87 (6), 3703-3715.
97. Mercier, C.; Masseguin, C.; Roux, F.; Gabrion, J.; Scherrmann, J. M. Expression of P-glycoprotein (ABCB1) and Mrp1 (ABCC1) in adult rat brain: focus on astrocytes. Brain Res., 2004, 1021 (1), 32-40.
98. Stride, B. D.; Grant, C. E.; Loe, D.W.; Hipfner, D. R.; Cole, S. P.; Deeley, R. G. Pharmacological characterization of the murine and human orthologs of multidrug-resistance protein in transfected human embryonic kidney cells. Mol. Pharmacol., 1997, 52 (3), 344-353.
99. Evers, R.; Kool, M.; Smith, A. J.; van Deemter, L.; de Haas, M.; Borst, P. Inhibitory effect of the reversal agents V-104, GF120918 and Pluronic L61 on MDR1 Pgp-, MRP1-and MRP2-mediated transport. Br. J. Cancer, 2000, 83 (3), 366-374.
100. Loe, D.W.; Almquist, K.C.; Deeley, R.G.; Cole, S.P. 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 (16), 9675-9682.
101. Rappa, G.; Lorico, A.; Flavell, R. A.; Sartorelli, A.C. Evidence that the multidrug resistance protein (MRP) functions as a cotransporter of glutathione and natural product toxins. Cancer Res., 1997, 57 (23), 5232-5237.
102. Renes, J.; De Vries, E. G.; Nienhuis, E.F.; Jansen, P. L.; Muller, M. ATP-and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Brit. J. Pharmacol., 1999, 126 (3), 681-688.
103. Grant, C.E.; Valdimarsson, G.; Hipfner, D. R.; Almquist, K.C.; Cole, S. P.; Deeley, R.G. Overexpression of multidrug resistance associated protein (MRP) increases resistance to natural product drugs. Cancer Res., 1994, 54 (2), 357-361.
104. Zaman, G. J.; Flens, M. J.; van Leusden, M. R.; de Haas, M.; Mulder, H. S.; Lankelma, J.; Pinedo, H.M.; Scheper, R.J.; Baas, F.; Broxterman, H. J.; et al. The human multidrug resistanceassociated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl. Acad. Sci. U S A., 1994, 91 (19), 8822-8826.
105. Lautier, D.; Canitrot, Y.; Deeley, R.G.; Cole, S.P. Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem. Pharmacol., 1996, 52 (7), 967-977.
106. Leite, D.F.; Echevarria-Lima, J.; Salgado, L.T.; Capella, M.A.; Calixto, J. B.; Rumjanek, V. M. In vivo and in vitro modulation of MDR molecules in murine thymocytes. Int. Immunopharmacol., 2006, 6 (2), 204-215.
107. Duffy, C.P. Worksite cholesterol screening and diet education programs. AAOHN. J., 1998, 46 (3), 147-153.
108. Sun, H.; Johnson, D.R.; Finch, R.A.; Sartorelli, A C.; Miller, D.W.; Elmquist, W.F. Transport of fluorescein in MDCKII-MRP1 transfected cells and mrp1-knockout mice. Biochem. Biophys. Res. Commun., 2001, 284 (4), 863-869.
109. Ma, S.L.; Hu, Y.P.; Wang, F.; Huang, Z C.; Chen, Y. F.; Wang, X. K.; Fu, L.W. Lapatinib antagonizes multidrug resistance-associated protein 1-mediated multidrug resistance by inhibiting its transport function. Mol. Med., 2014, 20, 390-399.
110. Rocha Gda, G.; Oliveira, R. R.; Kaplan, M.A.; Gattass, C.R. 3beta-Acetyl tormentic acid reverts MRP1/ABCC1 mediated cancer resistance through modulation of intracellular levels of GSH and inhibition of GST activity. Eur. J.Pharmacol., 2014, 741, 140-149.
111. Holm, P.S.; Dietel, M.; Krupp, G. Similar cleavage efficiencies of an oligoribonucleotide substrate and an mdr1 mRNA segment by a hammerhead ribozyme. Gene, 1995, 167 (1-2), 221-225.
112. Kiehntopf, M.; Brach, M.A.; Licht, T.; Petschauer, S.; Karawajew, L.; Kirschning, C.; Herrmann, F. Ribozyme-mediated cleavage of the MDR-1 transcript restores chemosensitivity in previously resistant cancer cells. EMBO. J., 1994, 13 (19), 4645-4652.
113. Tanaka, Y.; Slitt, A.L.; Leazer, T.M.; Maher, J.M.; Klaassen, C.D. Tissue distribution and hormonal regulation of the breast cancer resistance protein (Bcrp/Abcg2) in rats and mice. Biochem. Biophys. Res. Commun., 2005, 326 (1), 181-187.
114. Zhou, S.; Morris, J.J.; Barnes, Y.; Lan, L.; Schuetz, J.D.; Sorrentino, B.P. 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. U S A., 2002, 99(19), 12339-12344.
115. Wang, H.; Zhou, L.; Gupta, A.; Vethanayagam, R. R.; Zhang, Y.; Unadkat, J.D.; Mao, Q. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am. J. Physiol. Endocrinol. Metab., 2006, 290 (5), E798-807.
116. Zander, S.A.; Kersbergen, A.; Sol, W.; Gonggrijp, M.; Van de Wetering, K.; Jonkers, J.; Borst, P.; Rottenberg, S. Lack of ABCG2 shortens latency of BRCA1-deficient mammary tumors and this is not affected by genistein or resveratrol. Cancer. Prev. Res (Phila)., 2012, 5(8), 1053-1060.
117. Kodaira, H.; Kusuhara, H.; Ushiki, J.; Fuse, E.; Sugiyama, Y. Kinetic analysis of the cooperation of P-glycoprotein (P-gp/Abcb1) and breast cancer resistance protein (Bcrp/Abcg2) in limiting the brain and testis penetration of erlotinib, flavopiridol, and mitoxantrone. J. Pharmacol. Exp. Ther., 2010, 333 (3), 788-796.
118. Bakhsheshian, J.; Wei, B. R.; Chang, K. E.; Shukla, S.; Ambudkar, S. V.; Simpson, R.M.; Gottesman, M.M.; Hall, M.D. Bioluminescent imaging of drug efflux at the blood-brain barrier mediated by the transporter ABCG2. Proc. Natl. Acad. Sci. U S A., 2013, 110 (51), 20801-20806.
119. Allen, J.D.; Schinkel, A.H. Multidrug resistance and pharmacological protection mediated by the breast cancer resistance protein (BCRP/ABCG2). Mol. Cancer. Ther., 2002, 1 (6), 427-434.
120. Zander, S.A.; Sol, W.; Greenberger, L.; Zhang, Y.; Van Tellingen, O.; Jonkers, J.; Borst, P.; Rottenberg, S. EZN-2208 (PEG-SN38) overcomes ABCG2-mediated topotecan resistance in BRCA1-deficient mouse mammary tumors. PLoS One, 2012, 7 (9), e45248.
121. Yang, C.; Xiong, F.; Wang, J.; Dou, J.; Chen, J.; Chen, D.; Zhang, Y.; Luo, S.; Gu, N. Anti-ABCG2 monoclonal antibody in combination with paclitaxel nanoparticles against cancer stem-like cell activity in multiple myeloma. Nanomedicine (Lond), 2014, 9 (1), 45-60.
122. Tan, K.W.; Cooney, J.; Jensen, D.; Li, Y.; Paxton, J.W.; Birch, N.P.; Scheepens, A. Hop-derived prenylflavonoids are substrates and inhibitors of the efflux transporter breast cancer resistance protein (BCRP/ABCG2). Mol. Nutr. Food. Res., 2014, 58 (11), 2099-2110.
123. Huang, X. C.; Xiao, X.; Zhang, Y. K.; Talele, T. T.; Salim, A.A.; Chen, Z.S.; Capon, R.J. Lamellarin O, a pyrrole alkaloid from an Australian marine sponge, Ianthella sp., reverses BCRP mediated drug resistance in cancer cells. Mar. Drugs., 2014, 12 (7), 3818-3837.
124. Yang, B.; Ma, Y.F.; Liu, Y. Elevated expression of nrf-2 and abcg2 involved in multi-drug resistance of lung cancer sp cells. Drug Res (Stuttg)., 2014.
125. Rao DK, L.H., Ambudkar SV, Mayer M. A Combination of curcumin with either gramicidin or ouabain selectively kills cells that express the multidrug resistance-linked ABCG2 transporter. Biol. Chem., 2014, 289, 14.
126. Gotovdorj, T.; Lee, E.; Lim, Y.; Cha, E. J.; Kwon, D.; Hong, E.; Kim, Y.; Oh, M. Y. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induced cell-specific drug transporters with acquired cisplatin resistance in cisplatin sensitive cancer cells. J. Korean. Med. Sci., 2014, 29 (9), 1188-1198.
127. Mazur, C. S.; Marchitti, S. A.; Zastre, J. P-glycoprotein inhibition by the agricultural pesticide propiconazole and its hydroxylated metabolites: Implications for pesticide-drug interactions. Toxicol. Lett., 2014.