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Vol. 55, Issue 5, 929-937, May 1999
Deutsches Krebsforschungszentrum, Heidelberg, Germany
The multidrug resistance protein MRP1 functions as an ATP-dependent
conjugate export pump and confers multidrug resistance. We cloned MRP2
(symbol ABCC2), a MRP family member localized to the apical membrane of
polarized cells. Stable expression of MRP2 in transfected human
embryonic kidney (HEK-293) and Madin-Darby canine kidney (MDCK) cells
was enhanced by inhibitors of histone deacetylase. In polarized MDCK
cells, both rat and human MRP2 were sorted to the apical plasma
membrane. An antibody raised against the amino terminus of rat MRP2
recognized the recombinant protein on the apical surface of
nonpermeabilized cells, providing direct evidence for the extracellular
localization of the amino terminus of MRP2. ATP-dependent transport by
recombinant human and rat MRP2 was measured with membrane vesicles from
stably transfected cells. The Km value of
human MRP2 was 1.0 ± 0.1 µM for leukotriene C4 and
7.2 ± 0.7 µM for 17
-glucuronosyl estradiol; the
Km values of human MRP1 were 0.1 ± 0.02 µM for leukotriene C4 and 1.5 ± 0.3 µM for
17-glucoronosyl estradiol. Thus, the
conjugate-transporting ATPases MRP2 and MRP1 differ not only by
their domain-specific localization but also by their kinetic
properties. Drug resistance conferred by recombinant MRP2 was studied
in MDCK and HEK-293 cells using cell viability assays. Expression of
human and rat MRP2 enhanced the resistance of MDCK cells to etoposide
5.0-fold and 3.8-fold and to vincristine 2.3- and 6.0-fold,
respectively. Buthionine sulfoximine reduced resistance to these drugs.
Human MRP2 overexpressed in HEK-293 cells enhanced the resistance to etoposide (4-fold), cisplatin (10-fold), doxorubicin (7.8-fold), and
epirubicin (5-fold). These results demonstrate that MRP2 confers resistance to cytotoxic drugs.
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Z. P. Lin, D. R. Johnson, R. A. Finch, M. G. Belinsky, G. D. Kruh, and A. C. Sartorelli Comparative Study of the Importance of Multidrug Resistance-associated Protein 1 and P-Glycoprotein to Drug Sensitivity in Immortalized Mouse Embryonic Fibroblasts Mol. Cancer Ther., October 1, 2002; 1(12): 1105 - 1114. [Abstract] [Full Text] [PDF]
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Y.-M. Qian, C. E. Grant, C. J. Westlake, D.-W. Zhang, P. A. Lander, R. L. Shepard, A. H. Dantzig, S. P. C. Cole, and R. G. Deeley Photolabeling of Human and Murine Multidrug Resistance Protein 1 with the High Affinity Inhibitor [125I]LY475776 and Azidophenacyl-[35S]Glutathione J. Biol. Chem., September 13, 2002; 277(38): 35225 - 35231. [Abstract] [Full Text] [PDF]
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S. B. M. Fernandez, Z. Hollo, A. Kern, E. Bakos, P. A. Fischer, P. Borst, and R. Evers Role of the N-terminal Transmembrane Region of the Multidrug Resistance Protein MRP2 in Routing to the Apical Membrane in MDCKII Cells J. Biol. Chem., August 16, 2002; 277(34): 31048 - 31055. [Abstract] [Full Text] [PDF]
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Z.-S. Chen, K. Lee, S. Walther, R. B. Raftogianis, M. Kuwano, H. Zeng, and G. D. Kruh Analysis of Methotrexate and Folate Transport by Multidrug Resistance Protein 4 (ABCC4): MRP4 Is a Component of the Methotrexate Efflux System Cancer Res., June 1, 2002; 62(11): 3144 - 3150. [Abstract] [Full Text] [PDF]
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D.-W. Zhang, S. P. C. Cole, and R. G. Deeley Determinants of the Substrate Specificity of Multidrug Resistance Protein 1. ROLE OF AMINO ACID RESIDUES WITH HYDROGEN BONDING POTENTIAL IN PREDICTED TRANSMEMBRANE HELIX 17 J. Biol. Chem., May 31, 2002; 277(23): 20934 - 20941. [Abstract] [Full Text] [PDF]
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A. Ilias, Z. Urban, T. L. Seidl, O. Le Saux, E. Sinko, C. D. Boyd, B. Sarkadi, and A. Varadi Loss of ATP-dependent Transport Activity in Pseudoxanthoma Elasticum-associated Mutants of Human ABCC6 (MRP6) J. Biol. Chem., May 3, 2002; 277(19): 16860 - 16867. [Abstract] [Full Text] [PDF]
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A. Guo, W. Marinaro, P. Hu, and P. J. Sinko Delineating the Contribution of Secretory Transporters in the Efflux of Etoposide Using Madin-Darby Canine Kidney (MDCK) Cells Overexpressing P-Glycoprotein (Pgp), Multidrug Resistance-Associated Protein (MRP1), and Canalicular Multispecific Organic Anion Transporter (cMOAT) Drug Metab. Dispos., April 1, 2002; 30(4): 457 - 463. [Abstract] [Full Text] [PDF]
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M. Sasaki, H. Suzuki, K. Ito, T. Abe, and Y. Sugiyama Transcellular Transport of Organic Anions Across a Double-transfected Madin-Darby Canine Kidney II Cell Monolayer Expressing Both Human Organic Anion-transporting Polypeptide (OATP2/SLC21A6) and Multidrug Resistance-associated Protein 2 (MRP2/ABCC2) J. Biol. Chem., February 15, 2002; 277(8): 6497 - 6503. [Abstract] [Full Text] [PDF]
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N. J. Cherrington, D. P. Hartley, N. Li, D. R. Johnson, and C. D. Klaassen Organ Distribution of Multidrug Resistance Proteins 1, 2, and 3 (Mrp1, 2, and 3) mRNA and Hepatic Induction of Mrp3 by Constitutive Androstane Receptor Activators in Rats J. Pharmacol. Exp. Ther., January 1, 2002; 300(1): 97 - 104. [Abstract] [Full Text] [PDF]
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Y. Cui, J. Konig, and D. Keppler Vectorial Transport by Double-Transfected Cells Expressing the Human Uptake Transporter SLC21A8 and the Apical Export Pump ABCC2 Mol. Pharmacol., November 1, 2001; 60(5): 934 - 943. [Abstract] [Full Text] [PDF]
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P. Duesberg, R. Stindl, and R. Hehlmann Origin of multidrug resistance in cells with and without multidrug resistance genes: Chromosome reassortments catalyzed by aneuploidy PNAS, September 5, 2001; (2001) 201398998. [Abstract] [Full Text] [PDF]
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A. Yamada, K. Kawano, M. Koga, T. Matsumoto, and K. Itoh Multidrug Resistance-associated Protein 3 Is a Tumor Rejection Antigen Recognized by HLA-A2402-restricted Cytotoxic T Lymphocytes Cancer Res., September 1, 2001; 61(17): 6459 - 6466. [Abstract] [Full Text] [PDF]
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L. C. Young, B. G. Campling, S. P. C. Cole, R. G. Deeley, and J. H. Gerlach Multidrug Resistance Proteins MRP3, MRP1, and MRP2 in Lung Cancer: Correlation of Protein Levels with Drug Response and Messenger RNA Levels Clin. Cancer Res., June 1, 2001; 7(6): 1798 - 1804. [Abstract] [Full Text] [PDF]
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K. Ito, H. Suzuki, and Y. Sugiyama Charged Amino Acids in the Transmembrane Domains Are Involved in the Determination of the Substrate Specificity of Rat Mrp2 Mol. Pharmacol., April 16, 2001; 59(5): 1077 - 1085. [Abstract] [Full Text]
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L. Huang and M. Vore Multidrug Resistance P-Glycoprotein 2 Is Essential for the Biliary Excretion of Indocyanine Green Drug Metab. Dispos., April 13, 2001; 29(5): 634 - 637. [Abstract] [Full Text]
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K. Zhang, M. Chew, E. B. Yang, K. P. Wong, and P. Mack Modulation of Cisplatin Cytotoxicity and Cisplatin-Induced DNA Cross-Links in HepG2 Cells by Regulation of Glutathione-Related Mechanisms Mol. Pharmacol., April 1, 2001; 59(4): 837 - 843. [Abstract] [Full Text]
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D. Laouari, R. Yang, C. Veau, I. Blanke, and G. Friedlander Two apical multidrug transporters, P-gp and MRP2, are differently altered in chronic renal failure Am J Physiol Renal Physiol, April 1, 2001; 280(4): F636 - F645. [Abstract] [Full Text] [PDF]
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 K. Lee, A. J. P. Klein-Szanto, and G. D. Kruh Analysis of the MRP4 Drug Resistance Profile in Transfected NIH3T3 Cells J Natl Cancer Inst, December 6, 2000; 92(23): 1934 - 1940. [Abstract] [Full Text] [PDF]
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H. Xiong, K. C. Turner, E. S. Ward, P. L. M. Jansen, and K. L. R. Brouwer Altered Hepatobiliary Disposition of Acetaminophen Glucuronide in Isolated Perfused Livers from Multidrug Resistance-Associated Protein 2-Deficient TR- Rats J. Pharmacol. Exp. Ther., November 1, 2000; 295(2): 512 - 518. [Abstract] [Full Text]
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 M. V. St-Pierre, M. A. Serrano, R. I. R. Macias, U. Dubs, M. Hoechli, U. Lauper, P. J. Meier, and J. J. G. Marin Expression of members of the multidrug resistance protein family in human term placenta Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2000; 279(4): R1495 - R1503. [Abstract] [Full Text] [PDF]
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H. Zeng, G. Liu, P. A. Rea, and G. D. Kruh Transport of Amphipathic Anions by Human Multidrug Resistance Protein 3 Cancer Res., September 1, 2000; 60(17): 4779 - 4784. [Abstract] [Full Text]
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G. L. Scheffer, M. Kool, M. Heijn, Marcel de Haas, A. C. L. M. Pijnenborg, J. Wijnholds, A. van Helvoort, M. C. de Jong, J. H. Hooijberg, C. A. A. M. Mol, et al. Specific Detection of Multidrug Resistance Proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-Glycoprotein with a Panel of Monoclonal Antibodies Cancer Res., September 1, 2000; 60(18): 5269 - 5277. [Abstract] [Full Text]
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P. Borst, R. Evers, M. Kool, and J. Wijnholds A Family of Drug Transporters: the Multidrug Resistance-Associated Proteins J Natl Cancer Inst, August 16, 2000; 92(16): 1295 - 1302. [Abstract] [Full Text] [PDF]
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R. A. M. H. Van Aubel, R. Masereeuw, and F. G. M. Russel Molecular pharmacology of renal organic anion transporters Am J Physiol Renal Physiol, August 1, 2000; 279(2): F216 - F232. [Abstract] [Full Text] [PDF]
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J. Wijnholds, C. A. A. M. Mol, L. van Deemter, M. de Haas, G. L. Scheffer, F. Baas, J. H. Beijnen, R. J. Scheper, S. Hatse, E. De Clercq, et al. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs PNAS, June 6, 2000; (2000) 120159197. [Abstract] [Full Text]
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E. Hinoshita, T. Uchiumi, K.-i. Taguchi, N. Kinukawa, M. Tsuneyoshi, Y. Maehara, K. Sugimachi, and M. Kuwano Increased Expression of an ATP-binding Cassette Superfamily Transporter, Multidrug Resistance Protein 2, in Human Colorectal Carcinomas Clin. Cancer Res., June 1, 2000; 6(6): 2401 - 2407. [Abstract] [Full Text]
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G. L. Scheffer, M. Maliepaard, A. C. L. M. Pijnenborg, M. A. van Gastelen, M. C. de Jong, A. B. Schroeijers, D. M. van der Kolk, J. D. Allen, D. D. Ross, P. van der Valk, et al. Breast Cancer Resistance Protein Is Localized at the Plasma Membrane in Mitoxantrone- and Topotecan-resistant Cell Lines Cancer Res., May 1, 2000; 60(10): 2589 - 2593. [Abstract] [Full Text]
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T. Cantz, A. T. Nies, M. Brom, A. F. Hofmann, and D. Keppler MRP2, a human conjugate export pump, is present and transports fluo 3 into apical vacuoles of Hep G2 cells Am J Physiol Gastrointest Liver Physiol, April 1, 2000; 278(4): G522 - G531. [Abstract] [Full Text] [PDF]
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E. Bakos, R. Evers, E. Sinkó, A. Váradi, P. Borst, and B. Sarkadi Interactions of the Human Multidrug Resistance Proteins MRP1 and MRP2 with Organic Anions Mol. Pharmacol., April 1, 2000; 57(4): 760 - 768. [Abstract] [Full Text]
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T. Hirohashi, H. Suzuki, H. Takikawa, and Y. Sugiyama ATP-dependent Transport of Bile Salts by Rat Multidrug Resistance-associated Protein 3 (Mrp3) J. Biol. Chem., January 28, 2000; 275(4): 2905 - 2910. [Abstract] [Full Text] [PDF]
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J. Konig, Y. Cui, A. T. Nies, and D. Keppler A novel human organic anion transporting polypeptide localized to the basolateral hepatocyte membrane Am J Physiol Gastrointest Liver Physiol, January 1, 2000; 278(1): G156 - G164. [Abstract] [Full Text] [PDF]
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H. Zeng, L. J. Bain, M. G. Belinsky, and G. D. Kruh Expression of Multidrug Resistance Protein-3 (Multispecific Organic Anion Transporter-D) in Human Embryonic Kidney 293 Cells Confers Resistance to Anticancer Agents Cancer Res., December 1, 1999; 59(23): 5964 - 5967. [Abstract] [Full Text] [PDF]
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A. H. Dantzig, R. L. Shepard, K. L. Law, L. Tabas, S. Pratt, J. S. Gillespie, S. N. Binkley, M. T. Kuhfeld, J. J. Starling, and S. A. Wrighton Selectivity of the Multidrug Resistance Modulator, LY335979, for P-Glycoprotein and Effect on Cytochrome P-450 Activities J. Pharmacol. Exp. Ther., August 1, 1999; 290(2): 854 - 862. [Abstract] [Full Text]
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 T. P. SCHAUB, J. KARTENBECK, J. KÖNIG, H. SPRING, J. DÖRSAM, G. STAEHLER, S. STÖRKEL, W. F. THON, and D. KEPPLER Expression of the MRP2 Gene-Encoded Conjugate Export Pump in Human Kidney Proximal Tubules and in Renal Cell Carcinoma J. Am. Soc. Nephrol., June 1, 1999; 10(6): 1159 - 1169. [Abstract] [Full Text]
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J. Konig, Y. Cui, A. T. Nies, and D. Keppler Localization and Genomic Organization of a New Hepatocellular Organic Anion Transporting Polypeptide J. Biol. Chem., July 21, 2000; 275(30): 23161 - 23168. [Abstract] [Full Text] [PDF]
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G. Jedlitschky, B. Burchell, and D. Keppler The Multidrug Resistance Protein 5 Functions as an ATP-dependent Export Pump for Cyclic Nucleotides J. Biol. Chem., September 22, 2000; 275(39): 30069 - 30074. [Abstract] [Full Text] [PDF]
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