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[Cancer Research 59, 8-13, January 1, 1999]
© 1999 American Association for Cancer Research
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[Cancer Research 59, 8-13, January 1, 1999]
© 1999 American Association for Cancer Research

Advances in Brief

Molecular Cloning of cDNAs Which Are Highly Overexpressed in Mitoxantrone-resistant Cells

Demonstration of Homology to ABC Transport Genes

Keisuke Miyake, Lyn Mickley, Thomas Litman, Zhirong Zhan, Robert Robey, Barbara Cristensen, Mariafiorella Brangi, Lee Greenberger, Michael Dean, Tito Fojo and Susan E. Bates1

Medicine Branch, National Cancer Institute, NIH, Bethesda, Maryland 20892 [K. M., L. M., T. L., Z. Z., R. R., B. C., M. B., T. F., S. B.], Laboratory of Genomic Diversity, National Cancer Institute-Frederick Cancer Research and Development Center, Frederick, Maryland 21702 [M. D.], and Wyeth-Ayerst Pharmaceuticals, Pearl River, NY 19065 [L. G.]

Reports of multiple distinct mitoxantrone-resistant sublines without overexpression of P-glycoprotein or the multidrug-resistance associated protein have raised the possibility of the existence of another major transporter conferring drug resistance. In the present study, a cDNA library from mitoxantrone-resistant S1-M1-80 human colon carcinoma cells was screened by differential hybridization. Two cDNAs of different lengths were isolated and designated MXR1 and MXR2. Sequencing revealed a high degree of homology for the cDNAs with Expressed Sequence Tag sequences previously identified as belonging to an ATP binding cassette transporter. Homology to the Drosophila white gene and its homologues was found for the predicted amino acid sequence. Using either cDNA as a probe in a Northern analysis demonstrated high levels of expression in the S1-M1-80 cells and in the human breast cancer subline, MCF-7 AdVp3000. Levels were lower in earlier steps of selection, and in partial revertants. The gene is amplified 10–12-fold in the MCF-7 AdVp3000 cells, but not in the S1-M1-80 cells. These studies are consistent with the identification of a new ATP binding cassette transporter, which is overexpressed in mitoxantrone-resistant cells.




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T. Nakanishi, L. A. Doyle, B. Hassel, Y. Wei, K. S. Bauer, S. Wu, D. W. Pumplin, H.-B. Fang, and D. D. Ross
Functional Characterization of Human Breast Cancer Resistance Protein (BCRP, ABCG2) Expressed in the Oocytes of Xenopus laevis
Mol. Pharmacol., December 1, 2003; 64(6): 1452 - 1462.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. E. van Herwaarden, J. W. Jonker, E. Wagenaar, R. F. Brinkhuis, J. H. M. Schellens, J. H. Beijnen, and A. H. Schinkel
The Breast Cancer Resistance Protein (Bcrp1/Abcg2) Restricts Exposure to the Dietary Carcinogen 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine
Cancer Res., October 1, 2003; 63(19): 6447 - 6452.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. L. Volk and E. Schneider
Wild-Type Breast Cancer Resistance Protein (BCRP/ABCG2) is a Methotrexate Polyglutamate Transporter
Cancer Res., September 1, 2003; 63(17): 5538 - 5543.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
Y. Imai, S. Asada, S. Tsukahara, E. Ishikawa, T. Tsuruo, and Y. Sugimoto
Breast Cancer Resistance Protein Exports Sulfated Estrogens but Not Free Estrogens
Mol. Pharmacol., September 1, 2003; 64(3): 610 - 618.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Kawabata, M. Oka, H. Soda, K. Shiozawa, K. Nakatomi, J. Tsurutani, Y. Nakamura, S. Doi, T. Kitazaki, K. Sugahara, et al.
Expression and Functional Analyses of Breast Cancer Resistance Protein in Lung Cancer
Clin. Cancer Res., August 1, 2003; 9(8): 3052 - 3057.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Nakanishi, J. E. Karp, M. Tan, L. A. Doyle, T. Peters, W. Yang, D. Wei, and D. D. Ross
Quantitative Analysis of Breast Cancer Resistance Protein and Cellular Resistance to Flavopiridol in Acute Leukemia Patients
Clin. Cancer Res., August 1, 2003; 9(9): 3320 - 3328.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Z.-S. Chen, R. W. Robey, M. G. Belinsky, I. Shchaveleva, X.-Q. Ren, Y. Sugimoto, D. D. Ross, S. E. Bates, and G. D. Kruh
Transport of Methotrexate, Methotrexate Polyglutamates, and 17{beta}-Estradiol 17-({beta}-D-glucuronide) by ABCG2: Effects of Acquired Mutations at R482 on Methotrexate Transport
Cancer Res., July 15, 2003; 63(14): 4048 - 4054.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
A. C. Lockhart, R. G. Tirona, and R. B. Kim
Pharmacogenetics of ATP-binding Cassette Transporters in Cancer and Chemotherapy
Mol. Cancer Ther., July 1, 2003; 2(7): 685 - 698.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. Rajendra, M. K. Gounder, A. Saleem, J. H. M. Schellens, D. D. Ross, S. E. Bates, P. Sinko, and E. H. Rubin
Differential Effects of the Breast Cancer Resistance Protein on the Cellular Accumulation and Cytotoxicity of 9-Aminocamptothecin and 9-Nitrocamptothecin
Cancer Res., June 15, 2003; 63(12): 3228 - 3233.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Suzuki, H. Suzuki, Y. Sugimoto, and Y. Sugiyama
ABCG2 Transports Sulfated Conjugates of Steroids and Xenobiotics
J. Biol. Chem., June 13, 2003; 278(25): 22644 - 22649.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
X. Wang, T. Furukawa, T. Nitanda, M. Okamoto, Y. Sugimoto, S.-I. Akiyama, and M. Baba
Breast Cancer Resistance Protein (BCRP/ABCG2) Induces Cellular Resistance to HIV-1 Nucleoside Reverse Transcriptase Inhibitors
Mol. Pharmacol., January 1, 2003; 63(1): 65 - 72.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
Y. Sugimoto, S. Tsukahara, Y. Imai, Y. Sugimoto, K. Ueda, and T. Tsuruo
Reversal of Breast Cancer Resistance Protein-mediated Drug Resistance by Estrogen Antagonists and Agonists
Mol. Cancer Ther., January 1, 2003; 2(1): 105 - 112.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. H. Mossink, A. van Zon, E. Franzel-Luiten, M. Schoester, V. A. Kickhoefer, G. L. Scheffer, R. J. Scheper, P. Sonneveld, and E. A. C. Wiemer
Disruption of the Murine Major Vault Protein (MVP/LRP) Gene Does Not Induce Hypersensitivity to Cytostatics
Cancer Res., December 15, 2002; 62(24): 7298 - 7304.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Ozvegy, A. Varadi, and B. Sarkadi
Characterization of Drug Transport, ATP Hydrolysis, and Nucleotide Trapping by the Human ABCG2 Multidrug Transporter. MODULATION OF SUBSTRATE SPECIFICITY BY A POINT MUTATION
J. Biol. Chem., December 6, 2002; 277(50): 47980 - 47990.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
C.M.F. Kruijtzer, J.H. Beijnen, and J.H.M. Schellens
Improvement of Oral Drug Treatment by Temporary Inhibition of Drug Transporters and/or Cytochrome P450 in the Gastrointestinal Tract and Liver: An Overview
Oncologist, December 1, 2002; 7(6): 516 - 530.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. L. Volk, K. M. Farley, Y. Wu, F. Li, R. W. Robey, and E. Schneider
Overexpression of Wild-Type Breast Cancer Resistance Protein Mediates Methotrexate Resistance
Cancer Res., September 1, 2002; 62(17): 5035 - 5040.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
Y. Imai, M. Nakane, K. Kage, S. Tsukahara, E. Ishikawa, T. Tsuruo, Y. Miki, and Y. Sugimoto
C421A Polymorphism in the Human Breast Cancer Resistance Protein Gene Is Associated with Low Expression of Q141K Protein and Low-Level Drug Resistance
Mol. Cancer Ther., June 1, 2002; 1(8): 611 - 616.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
T. K. Bera, C. Iavarone, V. Kumar, S. Lee, B. Lee, and I. Pastan
MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer
PNAS, May 14, 2002; 99(10): 6997 - 7002.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. D. Allen, S. C. Jackson, and A. H. Schinkel
A Mutation Hot Spot in the Bcrp1 (Abcg2) Multidrug Transporter in Mouse Cell Lines Selected for Doxorubicin Resistance
Cancer Res., April 1, 2002; 62(8): 2294 - 2299.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
J. D. Allen, A. van Loevezijn, J. M. Lakhai, M. van der Valk, O. van Tellingen, G. Reid, J. H. M. Schellens, G.-J. Koomen, and A. H. Schinkel
Potent and Specific Inhibition of the Breast Cancer Resistance Protein Multidrug Transporter in Vitro and in Mouse Intestine by a Novel Analogue of Fumitremorgin C
Mol. Cancer Ther., April 1, 2002; 1(6): 417 - 425.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
J. D. Allen and A. H. Schinkel
Multidrug Resistance and Pharmacological Protection Mediated by the Breast Cancer Resistance Protein (BCRP/ABCG2)
Mol. Cancer Ther., April 1, 2002; 1(6): 427 - 434.
[Full Text] [PDF]

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 BloodHome page
C. W. Scharenberg, M. A. Harkey, and B. Torok-Storb
The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors
Blood, January 15, 2002; 99(2): 507 - 512.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Kim, H. Turnquist, J. Jackson, M. Sgagias, Y. Yan, M. Gong, M. Dean, J. G. Sharp, and K. Cowan
The Multidrug Resistance Transporter ABCG2 (Breast Cancer Resistance Protein 1) Effluxes Hoechst 33342 and Is Overexpressed in Hematopoietic Stem Cells
Clin. Cancer Res., January 1, 2002; 8(1): 22 - 28.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
G. Schmitz, T. Langmann, and S. Heimerl
Role of ABCG1 and other ABCG family members in lipid metabolism
J. Lipid Res., October 1, 2001; 42(10): 1513 - 1520.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Honjo, C. A. Hrycyna, Q.-W. Yan, W. Y. Medina-Perez, R. W. Robey, A. van de Laar, T. Litman, M. Dean, and S. E. Bates
Acquired Mutations in the MXR/BCRP/ABCP Gene Alter Substrate Specificity in MXR/BCRP/ABCP-overexpressing Cells
Cancer Res., September 1, 2001; 61(18): 6635 - 6639.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
P. Perego, M. De Cesare, P. De Isabella, N. Carenini, G. Beggiolin, G. Pezzoni, M. Palumbo, L. Tartaglia, G. Pratesi, C. Pisano, et al.
A Novel 7-modified Camptothecin Analog Overcomes Breast Cancer Resistance Protein-associated Resistance in a Mitoxantrone-selected Colon Carcinoma Cell Line
Cancer Res., August 1, 2001; 61(16): 6034 - 6037.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
M. Dean, Y. Hamon, and G. Chimini
The human ATP-binding cassette (ABC) transporter superfamily
J. Lipid Res., July 1, 2001; 42(7): 1007 - 1017.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Komatani, H. Kotani, Y. Hara, R. Nakagawa, M. Matsumoto, H. Arakawa, and S. Nishimura
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
Cancer Res., April 1, 2001; 61(7): 2827 - 2832.
[Abstract] [Full Text]

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 Cancer Res.Home page
M. Maliepaard, G. L. Scheffer, I. F. Faneyte, M. A. van Gastelen, A. C. L. M. Pijnenborg, A. H. Schinkel, M. J. van de Vijver, R. J. Scheper, and J. H. M. Schellens
Subcellular Localization and Distribution of the Breast Cancer Resistance Protein Transporter in Normal Human Tissues
Cancer Res., April 1, 2001; 61(8): 3458 - 3464.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
M. Maliepaard, M. A. van Gastelen, A. Tohgo, F. H. Hausheer, R. C. A. M. van Waardenburg, L. A. de Jong, D. Pluim, J. H. Beijnen, and J. H. M. Schellens
Circumvention of Breast Cancer Resistance Protein (BCRP)-mediated Resistance to Camptothecins in Vitro Using Non-Substrate Drugs or the BCRP Inhibitor GF120918
Clin. Cancer Res., April 1, 2001; 7(4): 935 - 941.
[Abstract] [Full Text]

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 Cancer Res.Home page
C. Erlichman, S. A. Boerner, C. G. Hallgren, R. Spieker, X.-Y. Wang, C. D. James, G. L. Scheffer, M. Maliepaard, D. D. Ross, K. C. Bible, et al.
The HER Tyrosine Kinase Inhibitor CI1033 Enhances Cytotoxicity of 7-Ethyl-10-hydroxycamptothecin and Topotecan by Inhibiting Breast Cancer Resistance Protein-mediated Drug Efflux
Cancer Res., January 1, 2001; 61(2): 739 - 748.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
R. W. Robey, W. Y. Medina-Pérez, K. Nishiyama, T. Lahusen, K. Miyake, T. Litman, A. M. Senderowicz, D. D. Ross, and S. E. Bates
Overexpression of the ATP-binding Cassette Half-Transporter, ABCG2 (MXR/BCRP/ABCP1), in Flavopiridol-resistant Human Breast Cancer Cells
Clin. Cancer Res., January 1, 2001; 7(1): 145 - 152.
[Abstract] [Full Text]

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 JNCI J Natl Cancer InstHome page
J. W. Jonker, J. W. Smit, R. F. Brinkhuis, M. Maliepaard, J. H. Beijnen, J. H. M. Schellens, and A. H. Schinkel
Role of Breast Cancer Resistance Protein in the Bioavailability and Fetal Penetration of Topotecan
J Natl Cancer Inst, October 18, 2000; 92(20): 1651 - 1656.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. D. Allen, R. F. Brinkhuis, L. v. Deemter, J. Wijnholds, and A. H. Schinkel
Extensive Contribution of the Multidrug Transporters P-Glycoprotein and Mrp1 to Basal Drug Resistance
Cancer Res., October 1, 2000; 60(20): 5761 - 5766.
[Abstract] [Full Text]

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 Cancer Res.Home page
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.
Specific Detection of Multidrug Resistance Proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-Glycoprotein with a Panel of Monoclonal Antibodies
Cancer Res., September 1, 2000; 60(18): 5269 - 5277.
[Abstract] [Full Text]

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 JNCI J Natl Cancer InstHome page
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.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. L. Volk, K. Rohde, M. Rhee, J. J. McGuire, L. A. Doyle, D. D. Ross, and E. Schneider
Methotrexate Cross-Resistance in a Mitoxantrone-selected Multidrug-resistant MCF7 Breast Cancer Cell Line Is Attributable to Enhanced Energy-dependent Drug Efflux
Cancer Res., July 1, 2000; 60(13): 3514 - 3521.
[Abstract] [Full Text]

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 BloodHome page
D. D. Ross, J. E. Karp, T. T. Chen, and L. A. Doyle
Expression of breast cancer resistance protein in blast cells from patients with acute leukemia
Blood, July 1, 2000; 96(1): 365 - 368.
[Abstract] [Full Text] [PDF]


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