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Volume 271, Number 16, Issue of April 19, 1996 pp. 9683-9689
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
ATP-dependent 17-Estradiol 17-(-

D

-Glucuronide) Transport by Multidrug Resistance Protein (MRP)

INHIBITION BY CHOLESTATIC STEROIDS

(Received for publication, November 30, 1995; and in revised form, January 29, 1996)

Douglas W. Loe Kurt C. Almquist Susan P. C. Cole Roger G. Deeley

In addition to its ability to confer resistance to a range of natural product type chemotherapeutic agents, multidrug resistance protein (MRP) has been shown to transport the cysteinyl leukotriene, LTC(4), and several other glutathione (GSH) S-conjugates. We now demonstrate that its range of potential physiological substrates also includes cholestatic glucuronidated steroids. ATP dependent, osmotically sensitive transport of the naturally occurring conjugated estrogen, 17beta-estradiol 17-(beta-D-glucuronide) (E(2)17betaG), was readily demonstrable in plasma membrane vesicles from populations of MRP-transfected HeLa cells (V(max) 1.4 nmol mg min, K 2.5 µM). The involvement of MRP was confirmed by demonstrating that transport was completely inhibited by a monoclonal antibody specific for an intracellular conformational epitope of the protein. MRP-mediated transport of LTC(4) was competitively inhibited by E(2)17betaG (K 22 µM), despite the lack of structural similarity between these two substrates. Competitive inhibition of [^3H]E(2)17betaG transport was also observed with a number of other cholestatic conjugated steroids. All of these compounds prevented photolabeling of MRP with [^3H]LTC(4), demonstrating that the cholestatic steroid and leukotriene conjugates compete either for the same or possibly overlapping sites on the protein. Consistent with the presence of overlapping but non-identical sites, studies using chemotherapeutic drugs to inhibit MRP-mediated E(2)17betaG transport indicated that daunorubicin had the highest relative potency of the drugs tested, whereas it was the least potent inhibitor of LTC(4) transport. Non-cholestatic steroids glucuronidated at the 3 position of the steroid nucleus, such as 17beta-estradiol 3-(beta-D-glucuronide), did not compete for transport of E(2)17betaG by MRP, nor did they inhibit photolabeling of the protein with [^3H]LTC(4). These data identify MRP as a potential transporter of cholestatic conjugated estrogens and demonstrate site-specific requirements for glucuronidation of the steroid nucleus.




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Using the National Cancer Institute Anticancer Drug Screen to Assess the Effect of MRP Expression on Drug Sensitivity Profiles
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[Abstract] [Full Text]


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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.
[Abstract] [Full Text] [PDF]


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M. Klein, E. Martinoia, and G. Weissenbock
Directly Energized Uptake of beta -Estradiol 17-(beta -D-Glucuronide) in Plant Vacuoles Is Strongly Stimulated by Glutathione Conjugates
J. Biol. Chem., January 2, 1998; 273(1): 262 - 270.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
X.-B. Chang, Y.-X. Hou, and J. R. Riordan
ATPase Activity of Purified Multidrug Resistance-associated Protein
J. Biol. Chem., December 5, 1997; 272(49): 30962 - 30968.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
C. Kast and P. Gros
Topology Mapping of the Amino-terminal Half of Multidrug Resistance-associated Protein by Epitope Insertion and Immunofluorescence
J. Biol. Chem., October 17, 1997; 272(42): 26479 - 26487.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
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.
[Abstract] [Full Text]


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Mol. Pharmacol.Home page
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.
[Abstract] [Full Text]


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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.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
D. W. Loe, K. C. Almquist, R. G. Deeley, and S. P. C. Cole
Multidrug Resistance Protein (MRP)-mediated Transport of Leukotriene C(4) and Chemotherapeutic Agents in Membrane Vesicles
J. Biol. Chem., April 19, 1996; 271(16): 9675 - 9682.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
K. Nagata, M. Nishitani, M. Matsuo, N. Kioka, T. Amachi, and K. Ueda
Nonequivalent Nucleotide Trapping in the Two Nucleotide Binding Folds of the Human Multidrug Resistance Protein MRP1
J. Biol. Chem., June 2, 2000; 275(23): 17626 - 17630.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
Y.-x. Hou, L. Cui, J. R. Riordan, and X.-b. Chang
Allosteric Interactions between the Two Non-equivalent Nucleotide Binding Domains of Multidrug Resistance Protein MRP1
J. Biol. Chem., June 30, 2000; 275(27): 20280 - 20287.
[Abstract] [Full Text] [PDF]


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Q. Mao, R. G. Deeley, and S. P. C. Cole
Functional Reconstitution of Substrate Transport by Purified Multidrug Resistance Protein MRP1 (ABCC1) in Phospholipid Vesicles
J. Biol. Chem., October 27, 2000; 275(44): 34166 - 34172.
[Abstract] [Full Text] [PDF]


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S. Ryu, T. Kawabe, S. Nada, and A. Yamaguchi
Identification of Basic Residues Involved in Drug Export Function of Human Multidrug Resistance-associated Protein 2
J. Biol. Chem., December 8, 2000; 275(50): 39617 - 39624.
[Abstract] [Full Text] [PDF]


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Y.-M. Qian, W.-C. Song, H. Cui, S. P. C. Cole, and R. G. Deeley
Glutathione Stimulates Sulfated Estrogen Transport by Multidrug Resistance Protein 1
J. Biol. Chem., February 23, 2001; 276(9): 6404 - 6411.
[Abstract] [Full Text] [PDF]


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G. Liu, R. Sanchez-Fernandez, Z.-S. Li, and P. A. Rea
Enhanced Multispecificity of Arabidopsis Vacuolar Multidrug Resistance-associated Protein-type ATP-binding Cassette Transporter, AtMRP2
J. Biol. Chem., March 16, 2001; 276(12): 8648 - 8656.
[Abstract] [Full Text] [PDF]


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D.-W. Zhang, S. P. C. Cole, and R. G. Deeley
Identification of an Amino Acid Residue in Multidrug Resistance Protein 1 Critical for Conferring Resistance to Anthracyclines
J. Biol. Chem., April 13, 2001; 276(16): 13231 - 13239.
[Abstract] [Full Text] [PDF]


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K.-i. Ito, S. L. Olsen, W. Qiu, R. G. Deeley, and S. P. C. Cole
Mutation of a Single Conserved Tryptophan in Multidrug Resistance Protein 1 (MRP1/ABCC1) Results in Loss of Drug Resistance and Selective Loss of Organic Anion Transport
J. Biol. Chem., May 4, 2001; 276(19): 15616 - 15624.
[Abstract] [Full Text] [PDF]


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E. M. Leslie, K.-i. Ito, P. Upadhyaya, S. S. Hecht, R. G. Deeley, and S. P. C. Cole
Transport of the beta -O-Glucuronide Conjugate of the Tobacco-specific Carcinogen 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) by the Multidrug Resistance Protein 1 (MRP1). REQUIREMENT FOR GLUTATHIONE OR A NON-SULFUR-CONTAINING ANALOG
J. Biol. Chem., July 20, 2001; 276(30): 27846 - 27854.
[Abstract] [Full Text] [PDF]


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Z.-S. Chen, K. Lee, and G. D. Kruh
Transport of Cyclic Nucleotides and Estradiol 17-beta -D-Glucuronide by Multidrug Resistance Protein 4. RESISTANCE TO 6-MERCAPTOPURINE AND 6-THIOGUANINE
J. Biol. Chem., August 31, 2001; 276(36): 33747 - 33754.
[Abstract] [Full Text] [PDF]


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D.-W. Zhang, S. P. C. Cole, and R. G. Deeley
Identification of a Nonconserved Amino Acid Residue in Multidrug Resistance Protein 1 Important for Determining Substrate Specificity. EVIDENCE FOR FUNCTIONAL INTERACTION BETWEEN TRANSMEMBRANE HELICES 14 AND 17
J. Biol. Chem., September 7, 2001; 276(37): 34966 - 34974.
[Abstract] [Full Text] [PDF]


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K.-i. Ito, C. J. Oleschuk, C. Westlake, M. Z. Vasa, R. G. Deeley, and S. P. C. Cole
Mutation of Trp1254 in the Multispecific Organic Anion Transporter, Multidrug Resistance Protein 2 (MRP2) (ABCC2), Alters Substrate Specificity and Results in Loss of Methotrexate Transport Activity
J. Biol. Chem., October 5, 2001; 276(41): 38108 - 38114.
[Abstract] [Full Text] [PDF]




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