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Science 23 February 1996:
Vol. 271. no. 5252, pp. 1126 - 1128
DOI: 10.1126/science.271.5252.1126
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Reports

Congenital Jaundice in Rats with a Mutation in a Multidrug Resistance-Associated Protein Gene

Coen C. Paulusma, * Piter J. Bosma, Guido J. R. Zaman, Conny T. M. Bakker, Marlies Otter, George L. Scheffer, Rik J. Scheper, Piet Borst, Ronald P. J. Oude Elferink

The human Dubin-Johnson syndrome and its animal model, the TR- rat, are characterized by a chronic conjugated hyperbilirubinemia. TR- rats are defective in the canalicular multispecific organic anion transporter (cMOAT), which mediates hepatobiliary excretion of numerous organic anions. The complementary DNA for rat cmoat, a homolog of the human multidrug resistance gene (hMRP1), was isolated and shown to be expressed in the canalicular membrane of hepatocytes. In the TR- rat, a single-nucleotide deletion in this gene resulted in a reduced messenger RNA level and absence of the protein. It is likely that this mutation accounts for the TR- phenotype.

C. C. Paulusma, P. J. Bosma, C. T. M. Bakker, R. P. J. Oude Elferink, Department of Gastrointestinal and Liver Diseases, Center for Liver and Intestinal Research, Academic Medical Center F0-116, Meibergdreef 9, 1105 AZ Amsterdam, Netherlands.
G. J. R. Zaman and P. Borst, Division of Molecular Biology, Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, Netherlands.
M. Otter, Department of Biochemistry, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, Netherlands.
G. L. Scheffer and R. J. Scheper, Department of Pathology, Free University Hospital, De Boelelaan 1117, 1080 HV Amsterdam, Netherlands.
* To whom correspondence should be addressed. E-mail: c.c.paulusma{at}amc.uva.nl


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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Physiol Rev 83, 633-671
   Abstract »    Full Text »    PDF »
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J. Biol. Chem. 276, 46400-46407
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Vectorial Transport by Double-Transfected Cells Expressing the Human Uptake Transporter SLC21A8 and the Apical Export Pump ABCC2.
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   Abstract »    Full Text »    PDF »
Increased Bioavailability of the Food-Derived Carcinogen 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in MRP2-Deficient Rats.
C. G. Dietrich, D. R. de Waart, R. Ottenhoff, I. G. Schoots, and R. P. J. O. Elferink (2001)
Mol. Pharmacol. 59, 974-980
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Charged Amino Acids in the Transmembrane Domains Are Involved in the Determination of the Substrate Specificity of Rat Mrp2.
K. Ito, H. Suzuki, and Y. Sugiyama (2001)
Mol. Pharmacol. 59, 1077-1085
   Abstract »    Full Text »
Identification of Breast Cancer Resistant Protein/Mitoxantrone Resistance/Placenta-Specific, ATP-binding Cassette Transporter as a Transporter of NB-506 and J-107088, Topoisomerase I Inhibitors with an Indolocarbazole Structure.
H. Komatani, H. Kotani, Y. Hara, R. Nakagawa, M. Matsumoto, H. Arakawa, and S. Nishimura (2001)
Cancer Res. 61, 2827-2832
   Abstract »    Full Text »
Two apical multidrug transporters, P-gp and MRP2, are differently altered in chronic renal failure.
D. Laouari, R. Yang, C. Veau, I. Blanke, and G. Friedlander (2001)
Am J Physiol Renal Physiol 280, F636-F645
   Abstract »    Full Text »    PDF »
IL-1-induced NFkappa B and c-Jun N-terminal kinase (JNK) activation diverge at IL-1 receptor-associated kinase (IRAK).
X. Li, M. Commane, Z. Jiang, and G. R. Stark (2001)
PNAS
   Abstract »    Full Text »
Cholestatic Potential of Troglitazone as a Possible Factor Contributing to Troglitazone-Induced Hepatotoxicity: In Vivo and in Vitro Interaction at the Canalicular Bile Salt Export Pump (Bsep) in the Rat.
C. Funk, C. Ponelle, G. Scheuermann, and M. Pantze (2001)
Mol. Pharmacol. 59, 627-635
   Abstract »    Full Text »
ATP-Binding Cassette Transporter ABC2/ABCA2 in the Rat Brain: A Novel Mammalian Lysosome-Associated Membrane Protein and a Specific Marker for Oligodendrocytes But Not for Myelin Sheaths.
C.-J. Zhou, L.-X. Zhao, N. Inagaki, J.-L. Guan, S. Nakajo, T. Hirabayashi, S. Kikuyama, and S. Shioda (2001)
J. Neurosci. 21, 849-857
   Abstract »    Full Text »    PDF »
Analysis of the MRP4 Drug Resistance Profile in Transfected NIH3T3 Cells.
K. Lee, A. J. P. Klein-Szanto, and G. D. Kruh (2000)
J Natl Cancer Inst 92, 1934-1940
   Abstract »    Full Text »    PDF »
Altered Hepatobiliary Disposition of Acetaminophen Glucuronide in Isolated Perfused Livers from Multidrug Resistance-Associated Protein 2-Deficient TR- Rats.
H. Xiong, K. C. Turner, E. S. Ward, P. L. M. Jansen, and K. L. R. Brouwer (2000)
J. Pharmacol. Exp. Ther. 295, 512-518
   Abstract »    Full Text »
The Effect of Rifampin Treatment on Intestinal Expression of Human MRP Transporters.
M. F. Fromm, H.-M. Kauffmann, P. Fritz, O. Burk, H. K. Kroemer, R. W. Warzok, M. Eichelbaum, W. Siegmund, and D. Schrenk (2000)
Am. J. Pathol. 157, 1575-1580
   Abstract »    Full Text »    PDF »
Cholate Resistance in Lactococcus lactis Is Mediated by an ATP-Dependent Multispecific Organic Anion Transporter.
A. Yokota, M. Veenstra, P. Kurdi, H. W. van Veen, and W. N. Konings (2000)
J. Bacteriol. 182, 5196-5201
   Abstract »    Full Text »
Transport of Amphipathic Anions by Human Multidrug Resistance Protein 3.
H. Zeng, G. Liu, P. A. Rea, and G. D. Kruh (2000)
Cancer Res. 60, 4779-4784
   Abstract »    Full Text »
Specific Detection of Multidrug Resistance Proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-Glycoprotein with a Panel of Monoclonal Antibodies.
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. (2000)
Cancer Res. 60, 5269-5277
   Abstract »    Full Text »
A Family of Drug Transporters: the Multidrug Resistance-Associated Proteins.
P. Borst, R. Evers, M. Kool, and J. Wijnholds (2000)
J Natl Cancer Inst 92, 1295-1302
   Abstract »    Full Text »    PDF »
Molecular pharmacology of renal organic anion transporters.
R. A. M. H. Van Aubel, R. Masereeuw, and F. G. M. Russel (2000)
Am J Physiol Renal Physiol 279, F216-F232
   Abstract »    Full Text »    PDF »
Pharmacokinetics and Hepatic Disposition of Bis[1-(ethoxycarbonyl)propyl]5-acetylamino-2,4,6-triiodoisophthalate in Rats and Isolated Perfused Rat Livers.
Y. Liu, E. R. Bacon, K. Ballinger, C. D. V. Black, K. Illig, G. L. McIntire, P. P. Wang, N. O'Neil, L. Kinter, and V. C. Desai (2000)
Drug Metab. Dispos. 28, 731-736
   Abstract »    Full Text »
The molecular genetics of familial intrahepatic cholestasis.
P L M JANSEN and M MULLER (2000)
Gut 47, 1-5
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Expression and Localization of Multidrug Resistant Protein mrp2 in Rat Small Intestine.
A. D. Mottino, T. Hoffman, L. Jennes, and M. Vore (2000)
J. Pharmacol. Exp. Ther. 293, 717-723
   Abstract »    Full Text »
Breast Cancer Resistance Protein Is Localized at the Plasma Membrane in Mitoxantrone- and Topotecan-resistant Cell Lines.
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. (2000)
Cancer Res. 60, 2589-2593
   Abstract »    Full Text »
Comparison of the Functional Characteristics of the Nucleotide Binding Domains of Multidrug Resistance Protein 1.
M. Gao, H.-R. Cui, D. W. Loe, C. E. Grant, K. C. Almquist, S. P. C. Cole, and R. G. Deeley (2000)
J. Biol. Chem. 275, 13098-13108
   Abstract »    Full Text »    PDF »
MRP2, a human conjugate export pump, is present and transports fluo 3 into apical vacuoles of Hep G2 cells.
T. Cantz, A. T. Nies, M. Brom, A. F. Hofmann, and D. Keppler (2000)
Am J Physiol Gastrointest Liver Physiol 278, G522-G531
   Abstract »    Full Text »    PDF »
Interactions of the Human Multidrug Resistance Proteins MRP1 and MRP2 with Organic Anions.
E. Bakos, R. Evers, E. Sinkó, A. Váradi, P. Borst, and B. Sarkadi (2000)
Mol. Pharmacol. 57, 760-768
   Abstract »    Full Text »
Transport Function and Hepatocellular Localization of mrp6 in Rat Liver.
J. Madon, B. Hagenbuch, L. Landmann, P. J. Meier, and B. Stieger (2000)
Mol. Pharmacol. 57, 634-641
   Abstract »    Full Text »
Function and Expression of Multidrug Resistance-Associated Protein Family in Human Colon Adenocarcinoma Cells (Caco-2).
T. Hirohashi, H. Suzuki, X.-Y. Chu, I. Tamai, A. Tsuji, and Y. Sugiyama (2000)
J. Pharmacol. Exp. Ther. 292, 265-270
   Abstract »    Full Text »
Involvement of an Organic Anion Transporter (Canalicular Multispecific Organic Anion Transporter/Multidrug Resistance-Associated Protein 2) in Gastrointestinal Secretion of Glutathione Conjugates in Rats.
Y. Gotoh, H. Suzuki, S. Kinoshita, T. Hirohashi, Y. Kato, and Y. Sugiyama (2000)
J. Pharmacol. Exp. Ther. 292, 433-439
   Abstract »    Full Text »
Expression of Multidrug Resistance Protein-3 (Multispecific Organic Anion Transporter-D) in Human Embryonic Kidney 293 Cells Confers Resistance to Anticancer Agents.
H. Zeng, L. J. Bain, M. G. Belinsky, and G. D. Kruh (1999)
Cancer Res. 59, 5964-5967
   Abstract »    Full Text »    PDF »
Differential regulation of canalicular multispecific organic anion transporter (cMOAT) expression by the chemopreventive agent oltipraz in primary rat hepatocytes and in rat liver.
A. Courtois, L. Payen, L. Vernhet, F. Morel, A. Guillouzo, and O. Fardel (1999)
Carcinogenesis 20, 2327-2330
   Abstract »    Full Text »    PDF »
Effect of Multidrug Resistance-Reversing Agents on Transporting Activity of Human Canalicular Multispecific Organic Anion Transporter.
Z.-S. Chen, T. Kawabe, M. Ono, S. Aoki, T. Sumizawa, T. Furukawa, T. Uchiumi, M. Wada, M. Kuwano, and S.-I. Akiyama (1999)
Mol. Pharmacol. 56, 1219-1228
   Abstract »    Full Text »


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