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[Cancer Research 61, 3458-3464, April 15, 2001]
© 2001 American Association for Cancer Research


Tumor Biology

Subcellular Localization and Distribution of the Breast Cancer Resistance Protein Transporter in Normal Human Tissues1

Marc Maliepaard2, George L. Scheffer2, Ian F. Faneyte, Margôt A. van Gastelen, Adriana C. L. M. Pijnenborg, Alfred H. Schinkel, Marc J. van de Vijver, Rik J. Scheper and Jan H. M. Schellens3

Divisions of Experimental Therapy [M. M., M. A. v. G., A. H. S., J. H. M. S.], Medical Oncology [J. H. M. S.], and Pathology [I. F. F., M. J. v. d. V.], The Netherlands Cancer Institute, 1066 CX Amsterdam; and Department of Pathology, Free University Hospital, 1081 HV Amsterdam [G. L. S., A. C. L. M. P., R. J. S.], the Netherlands

High expression of the Breast Cancer Resistance Protein (BCRP) gene has been shown to be involved in resistance to chemotherapeutic drugs. Knowledge of the localization of BCRP protein in normal tissues may help unravel the normal function of this protein. Therefore, we characterized the tissue distribution and cellular localization of BCRP in frozen sections of normal human tissues. For this purpose, we used the recently described monoclonal antibody BXP-34 and another independently developed monoclonal antibody directed against BCRP, BXP-21. Both monoclonal antibodies show specific BCRP plasma membrane staining on cytospins obtained from topotecan- or mitoxantrone-selected cell lines, as well as from BCRP-transfected cell lines. Immunoprecipitation experiments using either BXP-21 or BXP-34 yielded a clear Mr 72,000 BCRP band from BCRP-overexpressing tumor cells. In the topotecan-selected T8 and mitoxantrone-selected MX3 tumor cell lines, BCRP turned out to be differentially glycosylated. In contrast to BXP-34, BXP-21 is able to detect the Mr 72,000 BCRP protein on immunoblots and is reactive with BCRP in formalin-fixed, paraffin-embedded tissues.

Using BXP-21 and BXP-34, prominent staining of BCRP was observed in placental syncytiotrophoblasts, in the epithelium of the small intestine and colon, in the liver canalicular membrane, and in ducts and lobules of the breast. Furthermore, BCRP was present in veinous and capillary endothelium, but not in arterial endothelium in all of the tissues investigated. In the tissues studied, the mRNA levels of BCRP were assessed using reverse transcription-PCR, and these corresponded with the levels of BCRP protein estimated from immunohistochemical staining. The presence of BCRP at the placental syncytiotrophoblasts is consistent with the hypothesis of a protective role of BCRP for the fetus. The apical localization in the epithelium of the small intestine and colon indicates a possible role of BCRP in the regulation of the uptake of p.o. administered BCRP substrates by back-transport of substrate drugs entering from the gut lumen. Therefore, it may be useful to attempt to modulate the uptake of p.o. delivered BCRP substrates, e.g., topotecan or irinotecan, by using a BCRP inhibitor. Clinical trials testing this hypothesis have been initiated in our institute.




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Molecular Cancer TherapeuticsHome page
W. Chearwae, S. Shukla, P. Limtrakul, and S. V. Ambudkar
Modulation of the function of the multidrug resistance-linked ATP-binding cassette transporter ABCG2 by the cancer chemopreventive agent curcumin.
Mol. Cancer Ther., August 1, 2006; 5(8): 1995 - 2006.
[Abstract] [Full Text] [PDF]


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BloodHome page
T. Nakanishi, K. Shiozawa, B. A. Hassel, and D. D. Ross
Complex interaction of BCRP/ABCG2 and imatinib in BCR-ABL-expressing cells: BCRP-mediated resistance to imatinib is attenuated by imatinib-induced reduction of BCRP expression
Blood, July 15, 2006; 108(2): 678 - 684.
[Abstract] [Full Text] [PDF]


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International Journal of ToxicologyHome page
S. Choudhuri and C. D. Klaassen
Structure, Function, Expression, Genomic Organization, and Single Nucleotide Polymorphisms of Human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) Efflux Transporters
International Journal of Toxicology, July 1, 2006; 25(4): 231 - 259.
[Abstract] [Full Text] [PDF]


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Physiol. Rev.Home page
R. G. Deeley, C. Westlake, and S. P. C. Cole
Transmembrane Transport of Endo- and Xenobiotics by Mammalian ATP-Binding Cassette Multidrug Resistance Proteins.
Physiol Rev, July 1, 2006; 86(3): 849 - 899.
[Abstract] [Full Text] [PDF]


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Br J OphthalmolHome page
A Mohan, M Kandalam, H L Ramkumar, L Gopal, and S Krishnakumar
Stem cell markers: ABCG2 and MCM2 expression in retinoblastoma
Br J Ophthalmol, July 1, 2006; 90(7): 889 - 893.
[Abstract] [Full Text] [PDF]


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Pharmacol. Rev.Home page
L. Couture, J. A. Nash, and J. Turgeon
The ATP-Binding Cassette Transporters and Their Implication in Drug Disposition: A Special Look at the Heart.
Pharmacol. Rev., June 1, 2006; 58(2): 244 - 258.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
M. Leggas, J. C. Panetta, Y. Zhuang, J. D. Schuetz, B. Johnston, F. Bai, B. Sorrentino, S. Zhou, P. J. Houghton, and C. F. Stewart
Gefitinib Modulates the Function of Multiple ATP-Binding Cassette Transporters In vivo.
Cancer Res., May 1, 2006; 66(9): 4802 - 4807.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
H. Wang, L. Zhou, A. Gupta, R. R. Vethanayagam, Y. Zhang, J. D. Unadkat, and Q. Mao
Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells
Am J Physiol Endocrinol Metab, May 1, 2006; 290(5): E798 - E807.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
H. E. M. zu Schwabedissen, M. Grube, A. Dreisbach, G. Jedlitschky, K. Meissner, K. Linnemann, C. Fusch, C. A. Ritter, U. Volker, and H. K. Kroemer
EPIDERMAL GROWTH FACTOR-MEDIATED ACTIVATION OF THE MAP KINASE CASCADE RESULTS IN ALTERED EXPRESSION AND FUNCTION OF ABCG2 (BCRP)
Drug Metab. Dispos., April 1, 2006; 34(4): 524 - 533.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
K.-i. Nezasa, X. Tian, M. J. Zamek-Gliszczynski, N. J. Patel, T. J. Raub, and K. L. R. Brouwer
ALTERED HEPATOBILIARY DISPOSITION OF 5 (AND 6)-CARBOXY-2',7'-DICHLOROFLUORESCEIN IN Abcg2 (Bcrp1) AND Abcc2 (Mrp2) KNOCKOUT MICE
Drug Metab. Dispos., April 1, 2006; 34(4): 718 - 723.
[Abstract] [Full Text] [PDF]


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J. Histochem. Cytochem.Home page
K. Meissner, B. Heydrich, G. Jedlitschky, H. Meyer zu Schwabedissen, I. Mosyagin, P. Dazert, L. Eckel, S. Vogelgesang, R. W. Warzok, M. Bohm, et al.
The ATP-binding Cassette Transporter ABCG2 (BCRP), a Marker for Side Population Stem Cells, Is Expressed in Human Heart
J. Histochem. Cytochem., February 1, 2006; 54(2): 215 - 221.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
A. Swiatecka-Urban, A. Brown, S. Moreau-Marquis, J. Renuka, B. Coutermarsh, R. Barnaby, K. H. Karlson, T. R. Flotte, M. Fukuda, G. M. Langford, et al.
The Short Apical Membrane Half-life of Rescued {Delta}F508-Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Results from Accelerated Endocytosis of {Delta}F508-CFTR in Polarized Human Airway Epithelial Cells
J. Biol. Chem., November 4, 2005; 280(44): 36762 - 36772.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
U. Henriksen, J. U. Fog, T. Litman, and U. Gether
Identification of Intra- and Intermolecular Disulfide Bridges in the Multidrug Resistance Transporter ABCG2
J. Biol. Chem., November 4, 2005; 280(44): 36926 - 36934.
[Abstract] [Full Text] [PDF]


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CarcinogenesisHome page
B. Ebert, A. Seidel, and A. Lampen
Identification of BCRP as transporter of benzo[a]pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists
Carcinogenesis, October 1, 2005; 26(10): 1754 - 1763.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
A. Shafran, I. Ifergan, E. Bram, G. Jansen, I. Kathmann, G. J. Peters, R. W. Robey, S. E. Bates, and Y. G. Assaraf
ABCG2 Harboring the Gly482 Mutation Confers High-Level Resistance to Various Hydrophilic Antifolates
Cancer Res., September 15, 2005; 65(18): 8414 - 8422.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
S. Matsushima, K. Maeda, C. Kondo, M. Hirano, M. Sasaki, H. Suzuki, and Y. Sugiyama
Identification of the Hepatic Efflux Transporters of Organic Anions Using Double-Transfected Madin-Darby Canine Kidney II Cells Expressing Human Organic Anion-Transporting Polypeptide 1B1 (OATP1B1)/Multidrug Resistance-Associated Protein 2, OATP1B1/Multidrug Resistance 1, and OATP1B1/Breast Cancer Resistance Protein
J. Pharmacol. Exp. Ther., September 1, 2005; 314(3): 1059 - 1067.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
M. Hirano, K. Maeda, S. Matsushima, Y. Nozaki, H. Kusuhara, and Y. Sugiyama
Involvement of BCRP (ABCG2) in the Biliary Excretion of Pitavastatin
Mol. Pharmacol., September 1, 2005; 68(3): 800 - 807.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
M. J. Zamek-Gliszczynski, K. A. Hoffmaster, X. Tian, R. Zhao, J. W. Polli, J. E. Humphreys, L. O. Webster, A. S. Bridges, J. C. Kalvass, and K. L. R. Brouwer
MULTIPLE MECHANISMS ARE INVOLVED IN THE BILIARY EXCRETION OF ACETAMINOPHEN SULFATE IN THE RAT: ROLE OF MRP2 AND BCRP1
Drug Metab. Dispos., August 1, 2005; 33(8): 1158 - 1165.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
X.-f. Zhou, X. Yang, Q. Wang, R. A. Coburn, and M. E. Morris
EFFECTS OF DIHYDROPYRIDINES AND PYRIDINES ON MULTIDRUG RESISTANCE MEDIATED BY BREAST CANCER RESISTANCE PROTEIN: IN VITRO AND IN VIVO STUDIES
Drug Metab. Dispos., August 1, 2005; 33(8): 1220 - 1228.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
H. E. Meyer zu Schwabedissen, G. Jedlitschky, M. Gratz, S. Haenisch, K. Linnemann, C. Fusch, I. Cascorbi, and H. K. Kroemer
VARIABLE EXPRESSION OF MRP2 (ABCC2) IN HUMAN PLACENTA: INFLUENCE OF GESTATIONAL AGE AND CELLULAR DIFFERENTIATION
Drug Metab. Dispos., July 1, 2005; 33(7): 896 - 904.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
R. R. Vethanayagam, H. Wang, A. Gupta, Y. Zhang, F. Lewis, J. D. Unadkat, and Q. Mao
FUNCTIONAL ANALYSIS OF THE HUMAN VARIANTS OF BREAST CANCER RESISTANCE PROTEIN: I206L, N590Y, AND D620N
Drug Metab. Dispos., June 1, 2005; 33(6): 697 - 705.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
A. L. A. Sesink, I. C. W. Arts, V. C. J. de Boer, P. Breedveld, J. H. M. Schellens, P. C. H. Hollman, and F. G. M. Russel
Breast Cancer Resistance Protein (Bcrp1/Abcg2) Limits Net Intestinal Uptake of Quercetin in Rats by Facilitating Apical Efflux of Glucuronides
Mol. Pharmacol., June 1, 2005; 67(6): 1999 - 2006.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
N. Zelcer, K. van de Wetering, M. Hillebrand, E. Sarton, A. Kuil, P. R. Wielinga, T. Tephly, A. Dahan, J. H. Beijnen, and P. Borst
Mice lacking multidrug resistance protein 3 show altered morphine pharmacokinetics and morphine-6-glucuronide antinociception
PNAS, May 17, 2005; 102(20): 7274 - 7279.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
C. Q. Xia, N. Liu, D. Yang, G. Miwa, and L.-S. Gan
EXPRESSION, LOCALIZATION, AND FUNCTIONAL CHARACTERISTICS OF BREAST CANCER RESISTANCE PROTEIN IN CACO-2 CELLS
Drug Metab. Dispos., May 1, 2005; 33(5): 637 - 643.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
M. T. Budak, O. S. Alpdogan, M. Zhou, R. M. Lavker, M.A. M. Akinci, and J. M. Wolosin
Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells
J. Cell Sci., April 15, 2005; 118(8): 1715 - 1724.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
D. Kolwankar, D. D. Glover, J. A. Ware, and T. S. Tracy
EXPRESSION AND FUNCTION OF ABCB1 AND ABCG2 IN HUMAN PLACENTAL TISSUE
Drug Metab. Dispos., April 1, 2005; 33(4): 524 - 529.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
U. Henriksen, U. Gether, and T. Litman
Effect of Walker A mutation (K86M) on oligomerization and surface targeting of the multidrug resistance transporter ABCG2
J. Cell Sci., April 1, 2005; 118(7): 1417 - 1426.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
I. Ifergan, G. Jansen, and Y. G. Assaraf
Cytoplasmic Confinement of Breast Cancer Resistance Protein (BCRP/ABCG2) as a Novel Mechanism of Adaptation to Short-Term Folate Deprivation
Mol. Pharmacol., April 1, 2005; 67(4): 1349 - 1359.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
M. H.G.P. Raaijmakers, E. P.L.M. de Grouw, L. H.H. Heuver, B. A. van der Reijden, J. H. Jansen, R. J. Scheper, G. L. Scheffer, T. J.M. de Witte, and R. A.P. Raymakers
Breast Cancer Resistance Protein in Drug Resistance of Primitive CD34+38- Cells in Acute Myeloid Leukemia
Clin. Cancer Res., March 15, 2005; 11(6): 2436 - 2444.
[Abstract] [Full Text] [PDF]


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BloodHome page
S. Zhou, Y. Zong, P. A. Ney, G. Nair, C. F. Stewart, and B. P. Sorrentino
Increased expression of the Abcg2 transporter during erythroid maturation plays a role in decreasing cellular protoporphyrin IX levels
Blood, March 15, 2005; 105(6): 2571 - 2576.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
S. Zhang, X. Wang, K. Sagawa, and M. E. Morris
FLAVONOIDS CHRYSIN AND BENZOFLAVONE, POTENT BREAST CANCER RESISTANCE PROTEIN INHIBITORS, HAVE NO SIGNIFICANT EFFECT ON TOPOTECAN PHARMACOKINETICS IN RATS OR MDR1A/1B (-/-) MICE
Drug Metab. Dispos., March 1, 2005; 33(3): 341 - 348.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
K. F. K. Ejendal and C. A. Hrycyna
Differential Sensitivities of the Human ATP-Binding Cassette Transporters ABCG2 and P-Glycoprotein to Cyclosporin A
Mol. Pharmacol., March 1, 2005; 67(3): 902 - 911.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Y. Nakamura, M. Oka, H. Soda, K. Shiozawa, M. Yoshikawa, A. Itoh, Y. Ikegami, J. Tsurutani, K. Nakatomi, T. Kitazaki, et al.
Gefitinib ("Iressa", ZD1839), an Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor, Reverses Breast Cancer Resistance Protein/ABCG2-Mediated Drug Resistance
Cancer Res., February 15, 2005; 65(4): 1541 - 1546.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
C. Ozvegy-Laczka, G. Varady, G. Koblos, O. Ujhelly, J. Cervenak, J. D. Schuetz, B. P. Sorrentino, G.-J. Koomen, A. Varadi, K. Nemet, et al.
Function-dependent Conformational Changes of the ABCG2 Multidrug Transporter Modify Its Interaction with a Monoclonal Antibody on the Cell Surface
J. Biol. Chem., February 11, 2005; 280(6): 4219 - 4227.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Y. Imai, E. Ishikawa, S. Asada, and Y. Sugimoto
Estrogen-Mediated Post transcriptional Down-regulation of Breast Cancer Resistance Protein/ABCG2
Cancer Res., January 15, 2005; 65(2): 596 - 604.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
D. Kobayashi, I. Ieiri, T. Hirota, H. Takane, S. Maegawa, J. Kigawa, H. Suzuki, E. Nanba, M. Oshimura, N. Terakawa, et al.
FUNCTIONAL ASSESSMENT OF ABCG2 (BCRP) GENE POLYMORPHISMS TO PROTEIN EXPRESSION IN HUMAN PLACENTA
Drug Metab. Dispos., January 1, 2005; 33(1): 94 - 101.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
P. Pavek, G. Merino, E. Wagenaar, E. Bolscher, M. Novotna, J. W. Jonker, and A. H. Schinkel
Human Breast Cancer Resistance Protein: Interactions with Steroid Drugs, Hormones, the Dietary Carcinogen 2-Amino-1-methyl-6-phenylimidazo(4,5-b)pyridine, and Transport of Cimetidine
J. Pharmacol. Exp. Ther., January 1, 2005; 312(1): 144 - 152.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
H. E.U. Meyer zu Schwabedissen, M. Grube, B. Heydrich, K. Linnemann, C. Fusch, H. K. Kroemer, and G. Jedlitschky
Expression, Localization, and Function of MRP5 (ABCC5), a Transporter for Cyclic Nucleotides, in Human Placenta and Cultured Human Trophoblasts: Effects of Gestational Age and Cellular Differentiation
Am. J. Pathol., January 1, 2005; 166(1): 39 - 48.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
P.L. R. Ee, X. He, D. D. Ross, and W. T. Beck
Modulation of breast cancer resistance protein (BCRP/ABCG2) gene expression using RNA interference
Mol. Cancer Ther., December 1, 2004; 3(12): 1577 - 1584.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
F. Loganzo, M. Hari, T. Annable, X. Tan, D. B. Morilla, S. Musto, A. Zask, J. Kaplan, A. A. Minnick Jr., M. K. May, et al.
Cells resistant to HTI-286 do not overexpress P-glycoprotein but have reduced drug accumulation and a point mutation in {alpha}-tubulin
Mol. Cancer Ther., October 1, 2004; 3(10): 1319 - 1327.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
N. Mizuno, M. Suzuki, H. Kusuhara, H. Suzuki, K. Takeuchi, T. Niwa, J. W. Jonker, and Y. Sugiyama
IMPAIRED RENAL EXCRETION OF 6-HYDROXY-5,7-DIMETHYL-2-METHYLAMINO-4-(3-PYRIDYLMETHYL) BENZOTHIAZOLE (E3040) SULFATE IN BREAST CANCER RESISTANCE PROTEIN (BCRP1/ABCG2) KNOCKOUT MICE
Drug Metab. Dispos., September 1, 2004; 32(9): 898 - 901.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
K. Yanase, S. Tsukahara, S. Asada, E. Ishikawa, Y. Imai, and Y. Sugimoto
Gefitinib reverses breast cancer resistance protein-mediated drug resistance
Mol. Cancer Ther., September 1, 2004; 3(9): 1119 - 1125.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
F. A. de Jong, S. Marsh, R. H. J. Mathijssen, C. King, J. Verweij, A. Sparreboom, and H. L. McLeod
ABCG2 Pharmacogenetics: Ethnic Differences in Allele Frequency and Assessment of Influence on Irinotecan Disposition
Clin. Cancer Res., September 1, 2004; 10(17): 5889 - 5894.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
P. Breedveld, N. Zelcer, D. Pluim, O. Sonmezer, M. M. Tibben, J. H. Beijnen, A. H. Schinkel, O. van Tellingen, P. Borst, and J. H. M. Schellens
Mechanism of the Pharmacokinetic Interaction between Methotrexate and Benzimidazoles: Potential Role for Breast Cancer Resistance Protein in Clinical Drug-Drug Interactions
Cancer Res., August 15, 2004; 64(16): 5804 - 5811.
[Abstract] [Full Text] [PDF]




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