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[Cancer Research 56, 988-994, March 1, 1996]
© 1996 American Association for Cancer Research
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Transport of Glutathione, Glucuronate, and Sulfate Conjugates by the MRP Gene-encoded Conjugate Export Pump1

Gabriele Jedlitschky2, Inka Leier, Ulrike Buchholz, Karin Barnouin, Gerhart Kurz and Dietrich Keppler

Division of Tumor Biochemistry, Deutsches Krebsforschungszentrum, In Neuenheimer Feld 280, D-69120 Heidelberg, Germany [G. J., I. L., U. B., K. B., D. K.] and Department for Organic Chemistry and Biochemistry, University of Freiburg, D-79104 Freiburg, Germany [G. K.]

Previous studies have identified the ATP-dependent export of glutathione conjugates as a physiological function of the multidrug resistance protein (MRP). The involvement of MRP in the transport of endogenous and xenobiotic conjugates was investigated further using membrane vesicles from MRP-transfected HeLa cells. The ATP-dependent transport of the glutathione conjugates [3H]leukotriene C4, S-(2,4-dinitrophenyl)-[3H]glutathione, and 3H-labeled oxidized glutathione was characterized by determination of the transport efficiency Vmax:Km amounting to 1031, 114, and 7.1 ml x mg protein-1 x min-1, respectively. Additional endogenous substrates for MRP-mediated transport included the steroid conjugate 17ß-glucuronosyl [3H]estradiol and the bile salt conjugates [6{alpha}-14C]glucuronosylhyodeoxycholate and 3{alpha}-sulfatolithocholyl [3H]taurine. The Km value of MRP for 17ß-glucuronosyl [3H]estradiol was 1.5 ± 0.3 µM, with a Vmax:Km ratio of 42 ml x mg protein-1 x min-1, and a Ki value of 0.7 µM for the leukotriene receptor antagonist MK 571. MRP-mediated ATP-dependent transport was observed for the anticancer drug conjugates glucuronosyl [3H]etoposide and monochloro-mono[3H]glutathionyl melphalan, but not for unmodified [14C]doxorubicin, [3H]daunorubicin, or [3H]vinblastine. Our results establish that MRP functions as an ATP-dependent export pump not only for glutathione conjugates but also for glucuronidated and sulfated endogenous as well as exogenous compounds.

1 This work was supported in part by the Deutsche Forschungsgemeinschaft through SFB 352 (Heidelberg, Germany).

2 To whom requests for reprints should be addressed. Phone: +49/6221-422404; Fax: +49/6221-422402.

Received 11/ 1/95. Accepted 1/ 4/96.




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Cancer Res., July 1, 2001; 61(14): 5461 - 5467.
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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.
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D. R. Johnson, R. A. Finch, Z. P. Lin, C. J. Zeiss, and A. C. Sartorelli
The Pharmacological Phenotype of Combined Multidrug-Resistance mdr1a/1b- and mrp1-deficient Mice
Cancer Res., February 1, 2001; 61(4): 1469 - 1476.
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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.
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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.
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M.-A. Wioland, J. Fleury–Feith, P. Corlieu, F. Commo, G. Monceaux, J. Lacau-St-Guily, and J.-F. Bernaudin
CFTR, MDR1, and MRP1 Immunolocalization in Normal Human Nasal Respiratory Mucosa
J. Histochem. Cytochem., September 1, 2000; 48(9): 1215 - 1222.
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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.
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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.
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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.
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M. Gao, H.-R. Cui, D. W. Loe, C. E. Grant, K. C. Almquist, S. P. C. Cole, and R. G. Deeley
Comparison of the Functional Characteristics of the Nucleotide Binding Domains of Multidrug Resistance Protein 1
J. Biol. Chem., April 21, 2000; 275(17): 13098 - 13108.
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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.
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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.
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E Bakos, R Evers, G Calenda, G. Tusnady, G Szakacs, A Varadi, and B Sarkadi
Characterization of the amino-terminal regions in the human multidrug resistance protein (MRP1)
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M. L. O'Brien, B. Vulevic, S. Freer, J. Boyd, H. Shen, and K. D. Tew
Glutathione Peptidomimetic Drug Modulator of Multidrug Resistance-Associated Protein
J. Pharmacol. Exp. Ther., December 1, 1999; 291(3): 1348 - 1355.
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U.K. Walle and T. Walle
Transport of the cooked-food mutagen 2-amino-1-methyl-6-phenylimidazo-[4,5-b]pyridine (PhIP) across the human intestinal Caco-2 cell monolayer: role of efflux pumps
Carcinogenesis, November 1, 1999; 20(11): 2153 - 2157.
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M. Kitazono, T. Sumizawa, Y. Takebayashi, Z.-S. Chen, T. Furukawa, S. Nagayama, A. Tani, S. Takao, T. Aikou, and S.-i. Akiyama
Multidrug Resistance and the Lung Resistance-Related Protein in Human Colon Carcinoma SW-620 Cells
J Natl Cancer Inst, October 6, 1999; 91(19): 1647 - 1653.
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B. D. Stride, S. P. C. Cole, and R. G. Deeley
Localization of a Substrate Specificity Domain in the Multidrug Resistance Protein
J. Biol. Chem., August 6, 1999; 274(32): 22877 - 22883.
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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.
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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.
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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.
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D. R. Hipfner, Q. Mao, W. Qiu, E. M. Leslie, M. Gao, R. G. Deeley, and S. P. C. Cole
Monoclonal Antibodies That Inhibit the Transport Function of the 190-kDa Multidrug Resistance Protein, MRP. LOCALIZATION OF THEIR EPITOPES TO THE NUCLEOTIDE-BINDING DOMAINS OF THE PROTEIN
J. Biol. Chem., May 28, 1999; 274(22): 15420 - 15426.
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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.
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Y. Cui, J. König, U. Buchholz, H. Spring, I. Leier, and D. Keppler
Drug Resistance and ATP-Dependent Conjugate Transport Mediated by the Apical Multidrug Resistance Protein, MRP2, Permanently Expressed in Human and Canine Cells
Mol. Pharmacol., May 1, 1999; 55(5): 929 - 937.
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A. TOJO, T. SEKINE, N. NAKAJIMA, M. HOSOYAMADA, Y. KANAI, K. KIMURA, and H. ENDOU
Immunohistochemical Localization of Multispecific Renal Organic Anion Transporter 1 in Rat Kidney
J. Am. Soc. Nephrol., March 1, 1999; 10(3): 464 - 471.
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M. Kool, M. v. d. Linden, M. de Haas, F. Baas, and P. Borst
Expression of Human MRP6, a Homologue of the Multidrug Resistance Protein Gene MRP1, in Tissues and Cancer Cells
Cancer Res., January 1, 1999; 59(1): 175 - 182.
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J. F. Rebbeor, G. C. Connolly, M. E. Dumont, and N. Ballatori
ATP-dependent Transport of Reduced Glutathione on YCF1, the Yeast Orthologue of Mammalian Multidrug Resistance Associated Proteins
J. Biol. Chem., December 11, 1998; 273(50): 33449 - 33454.
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E. Bakos, R. Evers, G. Szakacs, G. E. Tusnady, E. Welker, K. Szabo, M. de Haas, L. van Deemter, P. Borst, A. Varadi, et al.
Functional Multidrug Resistance Protein (MRP1) Lacking the N-terminal Transmembrane Domain
J. Biol. Chem., November 27, 1998; 273(48): 32167 - 32175.
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M. Alvarez, R. Robey, V. Sandor, K. Nishiyama, Y. Matsumoto, K. Paull, S. Bates, and T. Fojo
Using the National Cancer Institute Anticancer Drug Screen to Assess the Effect of MRP Expression on Drug Sensitivity Profiles
Mol. Pharmacol., November 1, 1998; 54(5): 802 - 814.
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X.-B. Chang, Y.-X. Hou, and J. R. Riordan
Stimulation of ATPase Activity of Purified Multidrug Resistance-associated Protein by Nucleoside Diphosphates
J. Biol. Chem., September 11, 1998; 273(37): 23844 - 23848.
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J. Wijnholds, G. L. Scheffer, M. van der Valk, P. van der Valk, J. H. Beijnen, R. J. Scheper, and P. Borst
Multidrug Resistance Protein 1 Protects the Oropharyngeal Mucosal Layer and the Testicular Tubules against Drug-induced Damage
J. Exp. Med., September 7, 1998; 188(5): 797 - 808.
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D. S. Miller, R. Masereeuw, J. Henson, and K. J. Karnaky Jr.
Excretory transport of xenobiotics by dogfish shark rectal gland tubules
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 1998; 275(3): R697 - R705.
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C. S. Morrow, P. K. Smitherman, S. K. Diah, E. Schneider, and A. J. Townsend
Coordinated Action of Glutathione S-Transferases (GSTs) and Multidrug Resistance Protein 1 (MRP1) in Antineoplastic Drug Detoxification. MECHANISM OF GST A1-1- AND MRP1-ASSOCIATED RESISTANCE TO CHLORAMBUCIL IN MCF7 BREAST CARCINOMA CELLS
J. Biol. Chem., August 7, 1998; 273(32): 20114 - 20120.
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H. Kusuhara, H. Suzuki, M. Naito, T. Tsuruo, and Y. Sugiyama
Characterization of Efflux Transport of Organic Anions in a Mouse Brain Capillary Endothelial Cell Line
J. Pharmacol. Exp. Ther., June 1, 1998; 285(3): 1260 - 1265.
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M. Gao, M. Yamazaki, D. W. Loe, C. J. Westlake, C. E. Grant, S. P. C. Cole, and R. G. Deeley
Multidrug Resistance Protein. IDENTIFICATION OF REGIONS REQUIRED FOR ACTIVE TRANSPORT OF LEUKOTRIENE C4
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J.-M. Bréchot, I. Hurbain, A. Fajac, N. Daty, and J.-F. Bernaudin
Different Pattern of MRP Localization in Ciliated and Basal Cells from Human Bronchial Epithelium
J. Histochem. Cytochem., April 1, 1998; 46(4): 513 - 518.
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 Plant CellHome page
Y.-P. Lu, Z.-S. Li, Y. M. Drozdowicz, S. Hortensteiner, E. Martinoia, and P. A. Rea
AtMRP2, an Arabidopsis ATP Binding Cassette Transporter Able to Transport Glutathione S-Conjugates and Chlorophyll Catabolites: Functional Comparisons with AtMRP1
PLANT CELL, February 1, 1998; 10(2): 267 - 282.
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K. Ito, H. Suzuki, T. Hirohashi, K. Kume, T. Shimizu, and Y. Sugiyama
Functional Analysis of a Canalicular Multispecific Organic Anion Transporter Cloned from Rat Liver
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X.-B. Chang, Y.-X. Hou, and J. R. Riordan
ATPase Activity of Purified Multidrug Resistance-associated Protein
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D. R. Hipfner, K. C. Almquist, E. M. Leslie, J. H. Gerlach, C. E. Grant, R. G. Deeley, and S. P. C. Cole
Membrane Topology of the Multidrug Resistance Protein (MRP). A STUDY OF GLYCOSYLATION-SITE MUTANTS REVEALS AN EXTRACYTOSOLIC NH2 TERMINUS
J. Biol. Chem., September 19, 1997; 272(38): 23623 - 23630.
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B. D. Stride, C. E. Grant, D. W. Loe, D. R. Hipfner, S. P. C. Cole, and R. G. Deeley
Pharmacological Characterization of the Murine and Human Orthologs of Multidrug-Resistance Protein in Transfected Human Embryonic Kidney Cells
Mol. Pharmacol., September 1, 1997; 52(3): 344 - 353.
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 Pharmacol. Rev.Home page
H. E. d. Vries, J. Kuiper, A. G. d. Boer, T. J. C. V. Berkel, and D. D. Breimer
The Blood-Brain Barrier in Neuroinflammatory Diseases
Pharmacol. Rev., June 1, 1997; 49(2): 143 - 156.
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D. W. Loe, R. K. Stewart, T. E. Massey, R. G. Deeley, and S. P. C. Cole
ATP-Dependent Transport of Aflatoxin B1 and Its Glutathione Conjugates by the Product of the Multidrug Resistance Protein (MRP) Gene
Mol. Pharmacol., June 1, 1997; 51(6): 1034 - 1041.
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H. Ishizuka, K. Konno, H. Naganuma, K. Sasahara, Y. Kawahara, K. Niinuma, H. Suzuki, and Y. Sugiyama
Temocaprilat, a Novel Angiotensin-Converting Enzyme Inhibitor, is Excreted in Bile via an ATP-dependent Active Transporter (cMOAT) That is Deficient in Eisai Hyperbilirubinemic Mutant Rats (EHBR)
J. Pharmacol. Exp. Ther., March 1, 1997; 280(3): 1304 - 1311.
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M. Gao, D. W. Loe, C. E. Grant, S. P.C. Cole, and R. G. Deeley
Reconstitution of ATP-dependent Leukotriene C4 Transport by Co-expression of Both Half-molecules of Human Multidrug Resistance Protein in Insect Cells
J. Biol. Chem., November 1, 1996; 271(44): 27782 - 27787.
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