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Analysis of Expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, Homologues of the Multidrug Resistance-associated Protein Gene (MRP1), in Human Cancer Cell Lines¹

Division of Molecular Biology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam [M. K., M. d. H., P. B.]; Department of Pathology, Free University Hospital, 1081 HV Amsterdam [G. L. S., R. J. S.]; Department of Pediatric Gastroenterology and Laboratory for Metabolic Diseases, Wilhelmina Children's Hospital, 3501 CA Utrecht [M. J. T. v. E., J. A. J.]; and Department of Neurology, Academic Medical Center, 1105 AZ Amsterdam [F. B.], the Netherlands

By screening databases of human expressed sequence tags, we have identified three new homologues of MRP1, the gene encoding the multidrug resistance-associated protein, and cMOAT (or MRP2), the canalicular multispecific organic anion transporter gene. We call these new genes MRP3, MRP4, and MRP5. MRP3, like cMOAT, is mainly expressed in the liver. MRP4 is expressed only at very low levels in a few tissues, and MRP5, like MRP1, is expressed in almost every tissue tested. To assess a possible role of these new MRP homologues in multidrug or cisplatin resistance, a large set of resistant cell lines was examined for the (over)expression of MRP1, cMOAT, MRP3, MRP4, and MRP5. We find that even in cells selected for a low level of resistance, several MRP-related genes can be up-regulated simultaneously. However, MRP4 is not overexpressed in any of the cell lines we analyzed; MRP3 and MRP5 are only overexpressed in a few cell lines, and the RNA levels do not seem to correlate with resistance to either doxorubicin or cisplatin. cMOAT is substantially overexpressed in several cell lines, and cMOAT RNA levels correlate with cisplatin but not doxorubicin resistance in a subset of resistant cell lines. Our results emphasize the need for gene-specific blocks in gene expression to define which transporter contributes to resistance in each resistant cell line.

¹ This work was supported by a grant from the Dutch Cancer Society (to F. B. and P. B.).

² To whom requests for reprints should be addressed. Phone: 31-20-5122880; Fax: 31-20-6691383.

Received 1/27/97. Accepted 6/11/97.

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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]

				K. Ogawa, H. Suzuki, T. Hirohashi, T. Ishikawa, P. J. Meier, K. Hirose, T. Akizawa, M. Yoshioka, and Y. Sugiyama Characterization of inducible nature of MRP3 in rat liver Am J Physiol Gastrointest Liver Physiol, March 1, 2000; 278(3): G438 - G446. [Abstract] [Full Text] [PDF]

				J. Madon, B. Hagenbuch, L. Landmann, P. J. Meier, and B. Stieger Transport Function and Hepatocellular Localization of mrp6 in Rat Liver Mol. Pharmacol., March 1, 2000; 57(3): 634 - 641. [Abstract] [Full Text]

				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]

				T. Hirohashi, H. Suzuki, X.-Y. Chu, I. Tamai, A. Tsuji, and Y. Sugiyama Function and Expression of Multidrug Resistance-Associated Protein Family in Human Colon Adenocarcinoma Cells (Caco-2) J. Pharmacol. Exp. Ther., January 1, 2000; 292(1): 265 - 270. [Abstract] [Full Text]

				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]

				Z.-S. Chen, T. Kawabe, M. Ono, S. Aoki, T. Sumizawa, T. Furukawa, T. Uchiumi, M. Wada, M. Kuwano, and S.-I. Akiyama Effect of Multidrug Resistance-Reversing Agents on Transporting Activity of Human Canalicular Multispecific Organic Anion Transporter Mol. Pharmacol., December 1, 1999; 56(6): 1219 - 1228. [Abstract] [Full Text]

				R. A. M. H. Van Aubel, J. B. Koenderink, J. G. P. Peters, C. H. Van Os, and F. G. M. Russel Mechanisms and Interaction of Vinblastine and Reduced Glutathione Transport in Membrane Vesicles by the Rabbit Multidrug Resistance Protein Mrp2 Expressed in Insect Cells Mol. Pharmacol., October 1, 1999; 56(4): 714 - 719. [Abstract] [Full Text]

				H. J. G. Arts, D. Katsaros, E. G. E. de Vries, M. Massobrio, F. Genta, S. Danese, R. Arisio, R. J. Scheper, M. Kool, G. L. Scheffer, et al. Drug Resistance-associated Markers P-Glycoprotein, Multidrug Resistance-associated Protein 1, Multidrug Resistance-associated Protein 2, and Lung Resistance Protein as Prognostic Factors in Ovarian Carcinoma Clin. Cancer Res., October 1, 1999; 5(10): 2798 - 2805. [Abstract] [Full Text] [PDF]

				H. Ishizuka, K. Konno, T. Shiina, H. Naganuma, K. Nishimura, K. Ito, H. Suzuki, and Y. Sugiyama Species Differences in the Transport Activity for Organic Anions across the Bile Canalicular Membrane J. Pharmacol. Exp. Ther., September 1, 1999; 290(3): 1324 - 1330. [Abstract] [Full Text]

				M. Maliepaard, M. A. van Gastelen, L. A. de Jong, D. Pluim, R. C. A. M. van Waardenburg, M. C. Ruevekamp-Helmers, B. G. J. Floot, and J. H. M. Schellens Overexpression of the BCRP/MXR/ABCP Gene in a Topotecan-selected Ovarian Tumor Cell Line Cancer Res., September 1, 1999; 59(18): 4559 - 4563. [Abstract] [Full Text] [PDF]

				M. A. McAleer, M. A. Breen, N. L. White, and N. Matthews pABC11 (Also Known as MOAT-C and MRP5), a Member of the ABC Family of Proteins, Has Anion Transporter Activity but Does Not Confer Multidrug Resistance When Overexpressed in Human Embryonic Kidney 293 Cells J. Biol. Chem., August 13, 1999; 274(33): 23541 - 23548. [Abstract] [Full Text] [PDF]

				M. Cvetkovic, B. Leake, M. F. Fromm, G. R. Wilkinson, and R. B. Kim OATP and P-Glycoprotein Transporters Mediate the Cellular Uptake and Excretion of Fexofenadine Drug Metab. Dispos., August 1, 1999; 27(8): 866 - 871. [Abstract] [Full Text]

				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]

				N. Strazielle and J.-F. Ghersi-Egea Demonstration of a Coupled Metabolism-Efflux Process at the Choroid Plexus as a Mechanism of Brain Protection Toward Xenobiotics J. Neurosci., August 1, 1999; 19(15): 6275 - 6289. [Abstract] [Full Text] [PDF]

				J. Lankelma, H. Dekker, R. Fernandez Luque, S. Luykx, K. Hoekman, P. v. d. Valk, P. J. van Diest, and H. M. Pinedo Doxorubicin Gradients in Human Breast Cancer Clin. Cancer Res., July 1, 1999; 5(7): 1703 - 1707. [Abstract] [Full Text] [PDF]

				M. Kool, M. van der Linden, M. de Haas, G. L. Scheffer, J. M. L. de Vree, A. J. Smith, G. Jansen, G. J. Peters, N. Ponne, R. J. Scheper, et al. MRP3, an organic anion transporter able to transport anti-cancer drugs PNAS, June 8, 1999; 96(12): 6914 - 6919. [Abstract] [Full Text] [PDF]

				D. F. Ortiz, S. Li, R. Iyer, X. Zhang, P. Novikoff, and I. M. Arias MRP3, a new ATP-binding cassette protein localized to the canalicular domain of the hepatocyte Am J Physiol Gastrointest Liver Physiol, June 1, 1999; 276(6): G1493 - G1500. [Abstract] [Full Text] [PDF]

				J. H. Hooijberg, H. J. Broxterman, M. Kool, Y. G. Assaraf, G. J. Peters, P. Noordhuis, R. J. Scheper, P. Borst, H. M. Pinedo, and G. Jansen Antifolate Resistance Mediated by the Multidrug Resistance Proteins MRP1 and MRP2 Cancer Res., June 1, 1999; 59(11): 2532 - 2535. [Abstract] [Full Text] [PDF]

				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]

				T. Hirohashi, H. Suzuki, and Y. Sugiyama Characterization of the Transport Properties of Cloned Rat Multidrug Resistance-associated Protein 3 (MRP3) J. Biol. Chem., May 21, 1999; 274(21): 15181 - 15185. [Abstract] [Full Text] [PDF]

				S. P. C. Cole Re: Characterization of MOAT-C and MOAT-D, New Members of the MRP/cMOAT Subfamily of Transporter Proteins J Natl Cancer Inst, May 19, 1999; 91(10): 888 - 888. [Full Text] [PDF]

				G. D. Kruh and M. G. Belinsky RESPONSE: Re: Characterization of MOAT-C and MOAT-D, New Members' of the MRP/cMOAT Subfamily of Transporter Proteins J Natl Cancer Inst, May 19, 1999; 91(10): 888a - 889a. [Full Text] [PDF]

				K. Niinuma, Y. Kato, H. Suzuki, C. A. Tyson, V. Weizer, J. E. Dabbs, R. Froehlich, C. E. Green, and Y. Sugiyama Primary active transport of organic anions on bile canalicular membrane in humans Am J Physiol Gastrointest Liver Physiol, May 1, 1999; 276(5): G1153 - G1164. [Abstract] [Full Text] [PDF]

				N. H. Hendrikse, E. G. E. de Vries, L. Eriks-Fluks, W. T. A. van der Graaf, G. A. P. Hospers, A. T. M. Willemsen, W. Vaalburg, and E. J. F. Franssen A New in Vivo Method to Study P-Glycoprotein Transport in Tumors and the Blood-Brain Barrier Cancer Res., May 1, 1999; 59(10): 2411 - 2416. [Abstract] [Full Text] [PDF]