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S. Bates
Published 2003 · Biology

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Acquired drug resistance was first observed in a laboratory model in 1950, in mouse leukemic cells passaged in mice treated with 4-amino- N 10 -methyl-pteroylglutamic acid. Daunorubicin-selected resistant tumor cells were found to have energy-dependent transport of daunorubicin that could be inhibited by vinblastine, vincristine, and other anthracyclines. Further, selection of cells for resistance to vinblastine resulted in the same phenotype. Tumor cell lines that were selected in the laboratory for resistance to doxorubicin or vincristine became cross-resistant to structurally unrelated anticancer agents, displayed active outward drug efflux, and were characterized by increased expression of a 170 kDa cell membrane glycoprotein that became known as P170 or P-glycoprotein. As critical as this discovery of the first human ATP-binding cassette (ABC) transporter was, it was the observation that drug resistance could be reversed in vitro by several different compounds, including verapamil that brought Pgp into prominence as a potential target for improving cancer therapy. This chapter begins by reviewing the mammalian ABC transporters linked to multidrug resistance. It also reviews the progress that has been made in developing ABC transporters as clinical targets in anticancer therapy.
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A human canalicular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation.
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Cytogenetics and P-glycoprotein (PGP) are independent predictors of treatment outcome in acute myeloid leukemia (AML).
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Clinical trials of P-glycoprotein reversal in solid tumours.
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Quantitative analysis of multidrug resistance gene expression in human osteosarcomas.
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Double knockout of the MRP gene leads to increased drug sensitivity in vitro.
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A dose-finding and pharmacokinetic study of reversal of multidrug resistance with SDZ PSC 833 in combination with doxorubicin in patients with solid tumors.
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P-glycoprotein substrates and antagonists cluster into two distinct groups.
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Multidrug-resistant gene expression in small-cell lung cancer.
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Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state.
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Quantitative reverse transcriptase-polymerase chain reaction measured expression of MDR1 and MRP in primary breast carcinoma.
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A multidrug resistance transporter from human MCF-7 breast cancer cells.
L. Doyle (1998)
Immunohistochemical detection of multidrug resistance protein in human lung cancer and normal lung.
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Phase I and pharmacokinetic study of paclitaxel in combination with biricodar, a novel agent that reverses multidrug resistance conferred by overexpression of both MDR1 and MRP.
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P-glycoprotein shows strong catalytic cooperativity between the two nucleotide sites.
A. Senior (1998)
A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis
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R. Lacave (1998)
Multidrug resistance-associated protein and mutant p53 protein expression in non-small cell lung cancer.
Y. Oshika (1998)
Amplification of the ATP-binding cassette 2 transporter gene is functionally linked with enhanced efflux of estramustine in ovarian carcinoma cells.
N. Laing (1998)
The Sister of P-glycoprotein Represents the Canalicular Bile Salt Export Pump of Mammalian Liver*
Thomas Gerloff (1998)
Taxol resistance mediated by transfection of the liver-specific sister gene of P-glycoprotein.
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Prognostic role of clinical, pathological and biological characteristics in patients with locally advanced breast cancer.
A. Honkoop (1998)
Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione.
D. Loe (1998)
Expression of the Lung Resistance Protein Predicts Poor Outcome in De Novo Acute Myeloid Leukemia
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Co-expression of the MDR1 gene and HSP27 in human ovarian cancer.
J. Schneider (1998)
No evidence of significant activity of the multidrug resistance gene product in primary human breast cancer.
S. Hegewisch-Becker (1998)
A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance.
R. Allikmets (1998)
Multiple drug resistance parameter expression in ovarian cancer.
F. Joncourt (1998)
Phase II trial of dexverapamil and epirubicin in patients with non-responsive metastatic breast cancer.
M. Lehnert (1998)
A phase I/II trial of paclitaxel for non‐Hodgkin's lymphoma followed by paclitaxel plus quinine in drug‐resistant disease
T. Miller (1998)
Levels of multidrug resistance (MDR1) P-glycoprotein expression by human breast cancer correlate with in vitro resistance to taxol and doxorubicin.
E. Mechetner (1998)
Influence of the heterogeneity of P-glycoprotein expression on technetium-99m-MIBI uptake in breast cancer.
L. Kostakoglu (1998)
Multidrug resistance related genes and p53 expression in human non small cell lung cancer.
S. Galimberti (1998)
Dose-dependent effects of PSC 833 on its tissue distribution and on the biliary excretion of endogenous substrates in rats.
S. Song (1998)
Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C.
S. Rabindran (1998)
Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells.
Y. Cui (1999)
The ABCA subclass of mammalian transporters.
Cyril Broccardo (1999)
Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line.
M. Maliepaard (1999)
Rapid activation of MDR1 gene expression in human metastatic sarcoma after in vivo exposure to doxorubicin.
A. Abolhoda (1999)
Studies of Human MDR1-MDR2 Chimeras Demonstrate the Functional Exchangeability of a Major Transmembrane Segment of the Multidrug Transporter and Phosphatidylcholine Flippase
Yi Zhou (1999)
Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes.
K. Miyake (1999)
Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR), and potential for glucuronidation in MXR-expressing cells.
M. Brangi (1999)
Simultaneous activity of MRP1 and Pgp is correlated with in vitro resistance to daunorubicin and with in vivo resistance in adult acute myeloid leukemia.
O. Legrand (1999)
Significance of Multi‐Drug‐Resistant Proteins in Predicting Chemotherapy Response and Prognosis in Epithelial Ovarian Cancer *
Y. Yokoyama (1999)
Clinical pharmacokinetics of doxorubicin in combination with GF120918, a potent inhibitor of MDR1 P-glycoprotein.
A. Sparreboom (1999)
Structural, mechanistic and clinical aspects of MRP1.
D. Hipfner (1999)
Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2.
J. H. Hooijberg (1999)
MDR1 gene expression in primary and advanced breast cancer.
X. Yang (1999)
Drug resistance-associated markers P-glycoprotein, multidrug resistance-associated protein 1, multidrug resistance-associated protein 2, and lung resistance protein as prognostic factors in ovarian carcinoma.
H. Arts (1999)
Expression of multidrug resistance protein-related genes in lung cancer: correlation with drug response.
L. C. Young (1999)
Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR.
M. de Bruin (1999)
p53 and P-glycoprotein expression do not correlate with survival in nonsmall cell lung cancer: a long-term study and literature review.
A. Haque (1999)
MRP3, an organic anion transporter able to transport anti-cancer drugs.
M. Kool (1999)
Efflux of Rhodamine From CD56+ Cells as a Surrogate Marker for Reversal of P-Glycoprotein–Mediated Drug Efflux by PSC 833
R. Robey (1999)
ATP-Dependent efflux of CPT-11 and SN-38 by the multidrug resistance protein (MRP) and its inhibition by PAK-104P.
Z. Chen (1999)
Selectivity of the multidrug resistance modulator, LY335979, for P-glycoprotein and effect on cytochrome P-450 activities.
A. Dantzig (1999)
High levels of lung resistance related protein mRNA in leukaemic cells from patients with acute myelogenous leukaemia are associated with inferior response to chemotherapy and prior treatment with mitoxantrone
D. Xu (1999)
Do P-glycoprotein and major vault protein (MVP/LRP) expression correlate with in vitro daunorubicin resistance in acute myeloid leukemia?
H. Broxterman (1999)
Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents.
H. Zeng (1999)
Tc-99m-Sestamibi scanning with SDZ PSC 833 as a functional detection method for resistance modulation in patients with solid tumours
M. Bakker (1999)
Increased accumulation of doxorubicin and doxorubicinol in cardiac tissue of mice lacking mdr1a P-glycoprotein
J. Asperen (1999)
Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane
J. König (1999)
An inventory of the human ABC proteins.
I. Klein (1999)
MDR1 and thymidylate synthase (TS) gene expressions in advanced breast cancer: relationships to drug exposure, p53 mutations, and clinical outcome of the patients.
S. Lizard-Nacol (1999)
P‐glycoprotein, lung resistance‐related protein and multidrug resistance associated protein in de novo acute non‐lymphocytic leukaemias: biological and clinical implications
M. Michieli (1999)
Treatment of Refractory and Relapsed Acute Myelogenous Leukemia With Combination Chemotherapy Plus the Multidrug Resistance Modulator PSC 833 (Valspodar)
R. Advani (1999)
Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group Study.
C. Leith (1999)
Amplification of 4q21–q22 and the MXR gene in independently derived mitoxantrone‐resistant cell lines
T. Knutsen (2000)
Hepatic transport of bile salts.
G. Kullak-Ublick (2000)
MDR1 gene expression and outcome in osteosarcoma: a prospective, multicenter study.
J. Wunder (2000)
Phase I study of paclitaxel in combination with a multidrug resistance modulator, PSC 833 (Valspodar), in refractory malignancies.
P. Fracasso (2000)
Incidence of P-glycoprotein overexpression and multidrug resistance (MDR) reversal in adult soft tissue sarcoma.
H. Coley (2000)
Technetium-99m MIBI single photon emission computed tomography as an indicator of prognosis for patients with lung cancer —Preliminaly report—
T. Komori (2000)
P-glycoprotein and multidrug resistance protein activities in relation to treatment outcome in acute myeloid leukemia.
D. M. van der Kolk (2000)
Lung resistance-related protein/major vault protein and vaults in multidrug-resistant cancer
G. Scheffer (2000)
Phase I dose-finding and pharmacokinetic study of paclitaxel and carboplatin with oral valspodar in patients with advanced solid tumors.
A. Patnaik (2000)
Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance.
M. J. Newman (2000)
Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance.
J. Allen (2000)
Quickly predicting chemotherapy response to paclitaxel-based therapy in non-small cell lung cancer by early technetium-99m methoxyisobutylisonitrile chest single-photon-emission computed tomography.
C. Kao (2000)
ABC transporters in lipid transport.
P. Borst (2000)
Specific detection of multidrug resistance proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-glycoprotein with a panel of monoclonal antibodies.
G. Scheffer (2000)
Expression of mediated P-glycoprotein multidrug resistance related to Tc-99m MIBI scintimammography results.
S. Sun (2000)
The orally administered P-glycoprotein inhibitor R101933 does not alter the plasma pharmacokinetics of docetaxel.
L. van Zuylen (2000)
P-Glycoprotein inhibitor valspodar (PSC 833) increases the intracellular concentrations of daunorubicin in vivo in patients with P-glycoprotein-positive acute myeloid leukemia.
U. Tidefelt (2000)
P-glycoprotein expression is a marker for chemotherapy resistance and prognosis in advanced ovarian cancer.
M. Baekelandt (2000)
The homodimeric ATP‐binding cassette transporter LmrA mediates multidrug transport by an alternating two‐site (two‐cylinder engine) mechanism
Hendrik W. van Veen (2000)
The Multidrug Resistance Protein 5 Functions as an ATP-dependent Export Pump for Cyclic Nucleotides*
G. Jedlitschky (2000)
Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan.
J. Jonker (2000)
Expression of breast cancer resistance protein in blast cells from patients with acute leukemia
D. Ross (2000)
Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier.
J. Wijnholds (2000)
A phase I study of induction chemotherapy for older patients with newly diagnosed acute myeloid leukemia (AML) using mitoxantrone, etoposide, and the MDR modulator PSC 833: a southwest oncology group study 9617.
T. Chauncey (2000)
Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs.
J. Wijnholds (2000)
The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2).
T. Litman (2000)
A family of drug transporters: the multidrug resistance-associated proteins.
P. Borst (2000)
Expression of LRP and MDR1 in locally advanced breast cancer predicts axillary node invasion at the time of rescue mastectomy after induction chemotherapy
J. Schneider (2000)
A common pharmacophore for epothilone and taxanes: molecular basis for drug resistance conferred by tubulin mutations in human cancer cells.
Paraskevi Giannakakou (2000)
[Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome].
S. Toh (2000)
P-glycoprotein in primary acute myeloid leukemia and treatment outcome of idarubicin/cytosine arabinoside-based induction therapy
H. Broxterman (2000)
Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver.
B. Stieger (2000)
Expression of Functional Markers in Acute Nonlymphoblastic Leukemia
Kyungja Han (2000)
Comparative study of Tc-99m MIBI and TI-201 SPECT in predicting chemotherapeutic response in non-small-cell lung cancer.
Y. Nishiyama (2000)
Phase I Study of Intravenous PSC‐833 and Doxorubicin: Reversal of Multidrug Resistance
H. Minami (2001)
Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: correlation of protein levels with drug response and messenger RNA levels.
L. C. Young (2001)
A phase I trial of doxorubicin, paclitaxel, and valspodar (PSC 833), a modulator of multidrug resistance.
R. Advani (2001)
The human ATP-binding cassette (ABC) transporter superfamily.
M. Dean (2001)
Phase I study of infusional paclitaxel in combination with the P-glycoprotein antagonist PSC 833.
I. Chico (2001)
In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576.
P. Mistry (2001)
Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine.
Z. Chen (2001)
Acquired mutations in the MXR/BCRP/ABCP gene alter substrate specificity in MXR/BCRP/ABCP-overexpressing cells.
Yasumasa Honjo (2001)
Expression of Multidrug Resistance‐related Transporters in Human Breast Carcinoma
A. Kanzaki (2001)
Phase I/II trial of the multidrug-resistance modulator valspodar combined with cisplatin and doxorubicin in refractory ovarian cancer.
M. Baekelandt (2001)
Toxicological relevance of the multidrug resistance protein 1, MRP1 (ABCC1) and related transporters.
E. Leslie (2001)
Determining MDR1/P‐glycoprotein expression in breast cancer
I. F. Faneyte (2001)
Evaluation of chemoresistance markers in women with epithelial ovarian carcinoma.
B. Goff (2001)
Overexpression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells.
R. Robey (2001)
P-Glycoprotein and multidrug resistance-related protein expressions in relation to technetium-99m methoxyisobutylisonitrile scintimammography findings.
C. Kao (2001)
Phase I/II study of the P-glycoprotein modulator PSC 833 in patients with acute myeloid leukemia.
R. Dorr (2001)
Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues.
M. Maliepaard (2001)
Phase I and pharmacokinetic study of the novel MDR1 and MRP1 inhibitor biricodar administered alone and in combination with doxorubicin.
R. Peck (2001)
Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis.
R. Wang (2001)
Characterization of the Catalytic Cycle of ATP Hydrolysis by Human P-glycoprotein
Z. Sauna (2001)
Evaluation of chemotherapy response using technetium‐99M‐sestamibi scintigraphy in untreated adult malignant lymphomas and comparison with other prognosis factors: A preliminary report
C. Kao (2001)
Combined action of PSC 833 (Valspodar), a novel MDR reversing agent, with mitoxantrone, etoposide and cytarabine in poor-prognosis acute myeloid leukemia
G. Visani (2001)
T. Perri (2001)
An ATP-binding cassette gene (ABCG3) closely related to the multidrug transporter ABCG2 (MXR/ABCP) has an unusual ATP-binding domain
L. Mickley (2001)
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