© 2000 by Oxford University Press
Journal of the National Cancer Institute, Vol. 92, No. 16, 1295-1302,
August 16, 2000
© 2000 Oxford University Press
REVIEW |
A Family of Drug Transporters: the Multidrug Resistance-Associated Proteins
Affiliation of authors: Division of Molecular Biology and Center of Biomedical Genetics, The Netherlands Cancer Institute, Amsterdam.
Correspondence to: Piet Borst, M.D., Ph.D., Division of Molecular Biology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands (e-mail: pborst{at}nki.nl).
The human multidrug resistance-associated protein (MRP) family currently has seven members. The ability of several of these membrane proteins to transport a wide range of anticancer drugs out of cells and their presence in many tumors make them prime suspects in unexplained cases of drug resistance, although proof that they contribute to clinical drug resistance is still lacking. Recent studies have begun to clarify the function of the MRP family members. MRPs are organic anion transporters; i.e., they transport anionic drugs, exemplified by methotrexate, and neutral drugs conjugated to acidic ligands, such as glutathione (GSH), glucuronate, or sulfate. However, MRP1, MRP2, and MRP3 can also cause resistance to neutral organic drugs that are not known to be conjugated to acidic ligands by transporting these drugs together with free GSH. MRP1 can even confer resistance to arsenite and MRP2 to cisplatin, again probably by transporting these compounds in complexes with GSH. MRP4 overexpression is associated with high-level resistance to the nucleoside analogues 9-(2-phosphonylmethoxyethyl) adenine and azidothymidine, both of which are used as anti-human immunodeficiency virus drugs. MRPs may, therefore, also have a role in resistance against nucleoside analogues used in cancer chemotherapy. Mice without Mrp1, a high-affinity leukotriene C4 transporter, have an altered response to inflammatory stimuli but are otherwise healthy and fertile. MRP2 is the major transporter responsible for the secretion of bilirubin glucuronides into bile, and humans without MRP2 develop a mild liver disease known as the Dubin–Johnson syndrome. The physiologic functions of the other MRPs are not known. Whether long-term inhibition of MRPs in humans can be tolerated (assuming that suitable inhibitors will be found) remains to be determined.
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A. Haimeur, G. Conseil, R. G. Deeley, and S. P.C. Cole Mutations of Charged Amino Acids in or near the Transmembrane Helices of the Second Membrane Spanning Domain Differentially Affect the Substrate Specificity and Transport Activity of the Multidrug Resistance Protein MRP1 (ABCC1) Mol. Pharmacol., June 1, 2004; 65(6): 1375 - 1385. [Abstract] [Full Text] [PDF]
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M. K. Ozvaran, X. X. Cao, S. D. Miller, B. A. Monia, W. K. Hong, and W. R. Smythe Antisense oligonucleotides directed at the bcl-xl gene product augment chemotherapy response in mesothelioma Mol. Cancer Ther., May 1, 2004; 3(5): 545 - 550. [Abstract] [Full Text] [PDF]
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X.-Y. Chu, S.-E. W. Huskey, M. P. Braun, B. Sarkadi, D. C. Evans, and R. Evers Transport of Ethinylestradiol Glucuronide and Ethinylestradiol Sulfate by the Multidrug Resistance Proteins MRP1, MRP2, and MRP3 J. Pharmacol. Exp. Ther., April 1, 2004; 309(1): 156 - 164. [Abstract] [Full Text]
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K. Koike, G. Conseil, E. M. Leslie, R. G. Deeley, and S. P. C. Cole Identification of Proline Residues in the Core Cytoplasmic and Transmembrane Regions of Multidrug Resistance Protein 1 (MRP1/ABCC1) Important for Transport Function, Substrate Specificity, and Nucleotide Interactions J. Biol. Chem., March 26, 2004; 279(13): 12325 - 12336. [Abstract] [Full Text] [PDF]
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R. Qiu, T. F. Kalhorn, and J. T. Slattery ABCC2-Mediated Biliary Transport of 4-Glutathionylcyclophosphamide and Its Contribution to Elimination of 4-Hydroxycyclophosphamide in Rat J. Pharmacol. Exp. Ther., March 1, 2004; 308(3): 1204 - 1212. [Abstract] [Full Text] [PDF]
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 E. D. Kharasch, C. Hoffer, T. G. Altuntas, and D. Whittington Quinidine as a Probe for the Role of P-Glycoprotein in the Intestinal Absorption and Clinical Effects of Fentanyl J. Clin. Pharmacol., March 1, 2004; 44(3): 224 - 233. [Abstract] [Full Text] [PDF]
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J van der Heijden, M C de Jong, B A C Dijkmans, W F Lems, R Oerlemans, I Kathmann, G L Scheffer, R J Scheper, Y G Assaraf, and G Jansen Acquired resistance of human T cells to sulfasalazine: stability of the resistant phenotype and sensitivity to non-related DMARDs Ann Rheum Dis, February 1, 2004; 63(2): 131 - 137. [Abstract] [Full Text] [PDF]
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J van der Heijden, M C de Jong, B A C Dijkmans, W F Lems, R Oerlemans, I Kathmann, C G Schalkwijk, G L Scheffer, R J Scheper, and G Jansen Development of sulfasalazine resistance in human T cells induces expression of the multidrug resistance transporter ABCG2 (BCRP) and augmented production of TNF{alpha} Ann Rheum Dis, February 1, 2004; 63(2): 138 - 143. [Abstract] [Full Text] [PDF]
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P. K. Smitherman, A. J. Townsend, T. E. Kute, and C. S. Morrow Role of Multidrug Resistance Protein 2 (MRP2, ABCC2) in Alkylating Agent Detoxification: MRP2 Potentiates Glutathione S-Transferase A1-1-Mediated Resistance to Chlorambucil Cytotoxicity J. Pharmacol. Exp. Ther., January 1, 2004; 308(1): 260 - 267. [Abstract] [Full Text] [PDF]
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D. Steinbach, S. Wittig, G. Cario, S. Viehmann, A. Mueller, B. Gruhn, R. Haefer, F. Zintl, and A. Sauerbrey The multidrug resistance-associated protein 3 (MRP3) is associated with a poor outcome in childhood ALL and may account for the worse prognosis in male patients and T-cell immunophenotype Blood, December 15, 2003; 102(13): 4493 - 4498. [Abstract] [Full Text] [PDF]
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T. Litman, T. Skovsgaard, and W. D. Stein Pumping of Drugs by P-Glycoprotein: A Two-Step Process? J. Pharmacol. Exp. Ther., December 1, 2003; 307(3): 846 - 853. [Abstract] [Full Text] [PDF]
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S. Taniguchi, Y. Mochida, T. Uchiumi, T. Tahira, K. Hayashi, K. Takagi, M. Shimada, Y. Maehara, H. Kuwano, S. Kono, et al. Genetic polymorphism at the 5' regulatory region of multidrug resistance 1 (MDR1) and its association with interindividual variation of expression level in the colon Mol. Cancer Ther., December 1, 2003; 2(12): 1351 - 1359. [Abstract] [Full Text] [PDF]
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H. H. Yang, M. H. Ma, R. A. Vescio, and J. R. Berenson Overcoming Drug Resistance in Multiple Myeloma: The Emergence of Therapeutic Approaches to Induce Apoptosis J. Clin. Oncol., November 15, 2003; 21(22): 4239 - 4247. [Abstract] [Full Text] [PDF]
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J. B. Vaidyanathan and T. Walle Cellular Uptake and Efflux of the Tea Flavonoid (-)Epicatechin-3-gallate in the Human Intestinal Cell Line Caco-2 J. Pharmacol. Exp. Ther., November 1, 2003; 307(2): 745 - 752. [Abstract] [Full Text] [PDF]
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T. Brooks, H. Minderman, K. L. O'Loughlin, P. Pera, I. Ojima, M. R. Baer, and R. J. Bernacki Taxane-based reversal agents modulate drug resistance mediated by P-glycoprotein, multidrug resistance protein, and breast cancer resistance protein Mol. Cancer Ther., November 1, 2003; 2(11): 1195 - 1205. [Abstract] [Full Text] [PDF]
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M. C. de Jong, G. L. Scheffer, H. J. Broxterman, J. H. Hooijberg, J. W. Slootstra, R. H. Meloen, R. J. Kreitman, S. R. Husain, B. H. Joshi, R. K. Puri, et al. Multidrug-Resistant Tumor Cells Remain Sensitive to a Recombinant Interleukin-4-Pseudomonas Exotoxin, Except When Overexpressing the Multidrug Resistance Protein MRP1 Clin. Cancer Res., October 15, 2003; 9(13): 5009 - 5017. [Abstract] [Full Text] [PDF]
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 P. Dazert, K. Meissner, S. Vogelgesang, B. Heydrich, L. Eckel, M. Bohm, R. Warzok, R. Kerb, U. Brinkmann, E. Schaeffeler, et al. Expression and Localization of the Multidrug Resistance Protein 5 (MRP5/ABCC5), a Cellular Export Pump for Cyclic Nucleotides, in Human Heart Am. J. Pathol., October 1, 2003; 163(4): 1567 - 1577. [Abstract] [Full Text] [PDF]
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A. L. Slitt, N. J. Cherrington, J. M. Maher, and C. D. Klaassen INDUCTION OF MULTIDRUG RESISTANCE PROTEIN 3 IN RAT LIVER IS ASSOCIATED WITH ALTERED VECTORIAL EXCRETION OF ACETAMINOPHEN METABOLITES Drug Metab. Dispos., September 1, 2003; 31(9): 1176 - 1186. [Abstract] [Full Text] [PDF]
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J. M. Gallo, S. Li, P. Guo, K. Reed, and J. Ma The Effect of P-glycoprotein on Paclitaxel Brain and Brain Tumor Distribution in Mice Cancer Res., August 15, 2003; 63(16): 5114 - 5117. [Abstract] [Full Text] [PDF]
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E. Solary, B. Drenou, L. Campos, P. de Cremoux, F. Mugneret, P. Moreau, B. Lioure, A. Falkenrodt, B. Witz, M. Bernard, et al. Quinine as a multidrug resistance inhibitor: a phase 3 multicentric randomized study in adult de novo acute myelogenous leukemia Blood, August 15, 2003; 102(4): 1202 - 1210. [Abstract] [Full Text] [PDF]
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T. Li, K. Ito, and T. Horie Transport of fluorescein methotrexate by multidrug resistance-associated protein 3 in IEC-6 cells Am J Physiol Gastrointest Liver Physiol, August 8, 2003; 285(3): G602 - G610. [Abstract] [Full Text] [PDF]
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 T. D. Warner and J. A. Mitchell Nonsteroidal antiinflammatory drugs inhibiting prostanoid efflux: As easy as ABC? PNAS, August 5, 2003; 100(16): 9108 - 9110. [Full Text] [PDF]
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D. J. Seward, A. S. Koh, J. L. Boyer, and N. Ballatori Functional Complementation between a Novel Mammalian Polygenic Transport Complex and an Evolutionarily Ancient Organic Solute Transporter, OST{alpha}-OST{beta} J. Biol. Chem., July 18, 2003; 278(30): 27473 - 27482. [Abstract] [Full Text] [PDF]
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A. Nzila, E. Mberu, P. Bray, G. Kokwaro, P. Winstanley, K. Marsh, and S. Ward Chemosensitization of Plasmodium falciparum by Probenecid In Vitro Antimicrob. Agents Chemother., July 1, 2003; 47(7): 2108 - 2112. [Abstract] [Full Text] [PDF]
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A. C. Lockhart, R. G. Tirona, and R. B. Kim Pharmacogenetics of ATP-binding Cassette Transporters in Cancer and Chemotherapy Mol. Cancer Ther., July 1, 2003; 2(7): 685 - 698. [Abstract] [Full Text] [PDF]
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U. Schroeder, K. M. Bernt, B. Lange, J. Wenkel, J. Jikai, D. Shabat, R. Amir, N. Huebener, A. G. Niethammer, C. Hagemeier, et al. Hydrolytically activated etoposide prodrugs inhibit MDR-1 function and eradicate established MDR-1 multidrug-resistant T-cell leukemia Blood, July 1, 2003; 102(1): 246 - 253. [Abstract] [Full Text] [PDF]
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N. Zelcer, M. T. Huisman, G. Reid, P. Wielinga, P. Breedveld, A. Kuil, P. Knipscheer, J. H. M. Schellens, A. H. Schinkel, and P. Borst Evidence for Two Interacting Ligand Binding Sites in Human Multidrug Resistance Protein 2 (ATP Binding Cassette C2) J. Biol. Chem., June 20, 2003; 278(26): 23538 - 23544. [Abstract] [Full Text] [PDF]
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M. Suzuki, H. Suzuki, Y. Sugimoto, and Y. Sugiyama ABCG2 Transports Sulfated Conjugates of Steroids and Xenobiotics J. Biol. Chem., June 13, 2003; 278(25): 22644 - 22649. [Abstract] [Full Text] [PDF]
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S. Wang, D. P. Hartley, S. L. Ciccotto, S. H. Vincent, R. B. Franklin, and M.-S. Kim INDUCTION OF HEPATIC PHASE II DRUG-METABOLIZING ENZYMES BY 1,7-PHENANTHROLINE IN RATS IS ACCOMPANIED BY INDUCTION OF MRP3 Drug Metab. Dispos., June 1, 2003; 31(6): 773 - 775. [Abstract] [Full Text] [PDF]
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F. Mayer, F. Honecker, L. H. J. Looijenga, and C. Bokemeyer Towards an understanding of the biological basis of response to cisplatin-based chemotherapy in germ-cell tumors Ann. Onc., June 1, 2003; 14(6): 825 - 832. [Abstract] [Full Text] [PDF]
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S L Hider, C Morgan, E Bell, I N Bruce, P Ranganathan, and H L McLeod Will pharmacogenetics allow better prediction of methotrexate toxicity and efficacy in patients with RA? Ann Rheum Dis, June 1, 2003; 62(6): 591 - 591. [Full Text] [PDF]
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