Metabolism of ATP-binding cassette drug transporter inhibitors: complicating factor for multidrug resistance

Bibliography

• GOTTESMAN MM: Mechanisms of cancer drug resistance. Ann. Rev. Med. (2002) 53:615–627.
   PubMed Web of Science ®Google Scholar
• BORST P, EVERS R, KOOL M, WIJNHOLDS J: A family of drug transporters: the multidrug resistanceassociated proteins. J. Natl. Cancer Inst. (2000) 92:1295–1302.
   PubMed Web of Science ®Google Scholar
• BORST P, ELFERINK RO: Mammalian ABC transporters in health and disease. Ann. Rev. Biochem. (2002) 71:537–592.
   PubMed Web of Science ®Google Scholar
• LOCKHART AC, TIRONA RG, KIM RB: Pharmacogenetics of ATP-binding cassette transporters in cancer and chemotherapy. Mol. Cancer Ther. (2003) 2:685–698.
   PubMed Web of Science ®Google Scholar
• DANTZIG AH, DE ALWIS DP, BURGESS M: Considerations in the design and development of transport inhibitors as adjuncts to drug therapy. Adv. Drug Deliv. Rev. (2003) 55:133–150.
   PubMed Web of Science ®Google Scholar
• BORGES-WALMSLEY MI, MCKEEGAN KS, WALMSLEY AR: Structure and function of efflux pumps that confer resistance to drugs. Biochem. J. (2003) 376:313–338.
   PubMed Web of Science ®Google Scholar
• LITMAN T, DRULEY TE, STEIN WD, BATES SE: From MDR to MXR: new understanding of multidrug resistance systems, their properties and clinical significance. Cell. Mol. Life Sci. (2001) 58:931–959.
   PubMed Web of Science ®Google Scholar
• LEONARD GD, POLGAR O, BATES SE: ABC transporters and inhibitors: new targets, new agents. Curr. Opin. Invest. Drugs (2002) 3:1652–1659.
   PubMedGoogle Scholar
• JULIANO RL, LING V: A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta (1976) 455:152–162.
   PubMed Web of Science ®Google Scholar
• UEDA K, CLARK DP, CHEN CJ, ROBINSON IB, GOTTESMAN MM, PASTAN I: The human multidrug resistance (mdr1) gene. J. Biol. Chem. (1987) 262:505–508.
   PubMed Web of Science ®Google Scholar
• RAMACHANDRA M, AMBUDKAR SV, CHEN D et al.: Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry (1998) 37:5010–5019.
   PubMed Web of Science ®Google Scholar
• SAUNA ZE, AMBUDKAR SV: Characterization of the catalytic cycle of ATP hydrolysis by human P-glycoprotein; the two ATP hydrolysis events in a single catalytic cycle are kinetically similar, but affect different functional outcomes. J. Biol. Chem. (2001) 276:11653–11661.
   PubMed Web of Science ®Google Scholar
• VEEN VAN HW, HIGGINS CF, KONINGS WN: Multidrug transport by ATP binding cassette transporters: a proposed two-cylinder engine mechanism. Res. Microbiology (2001) 152:365–374.
   PubMed Web of Science ®Google Scholar
• HOLLAND IB, COLE SPC, KUCHLER K, HIGGINS CF: Bacteria to Man, chapter V. In: Substrate-binding sites in ABC transporters. Hendrik W van Veen, R Callaghan (Eds), Academic Press, Elsevier Science Ltd,US (2003).
   Google Scholar
• FROMM MF, KIM RB, STEIN CM, WILKINSON GR, RODEN DM: Inhibition of P-glycoprotein-mediated drug transport: a unifying mechanism to explain the interaction between digoxin and quinidine. Circulation (1999) 99:552–557.
   PubMed Web of Science ®Google Scholar
• POLLI JW, WRING SA, HUMPHREYS JE et al.: Rational use of in vitro P-glycoprotein assays in drug discovery. J. Pharmacol. Exp. Ther. (2001) 299:620–628.
   PubMed Web of Science ®Google Scholar
• KIM RB, FROMM MF, WANDEL B et al.: The drug transporter P-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J. Clin. Invest. (1998) 101:289–294.
   PubMed Web of Science ®Google Scholar
• ALSENZ J, STEFFEN H, ALEX R: Active apical secretory efflux of the HIV protease inhibitors saquinovir and ritonavir in Caco-2 cell monolayers. Pharm. Res. (1998) 15:423–428.
   PubMed Web of Science ®Google Scholar
• SCHUETZ EG, YASUDA K, ARIMORI K, SCHUETZ JD: Human MDR1 and mouse mdr1a P-glycoprotein alter the cellular retention and disposition of erythromycin, but not of retinoic acid or benzo(a)pyrene. Arch Biochem. Biophys. (1998) 350:340–347.
   PubMed Web of Science ®Google Scholar
• SAEKI T, UEDA K, TANIGAWARA Y, HORI R, KOMANO T: Human P-glycoprotein transports cyclosporin A and FK506. J. Biol Chem. (1993) 268:6077–6080.
   PubMed Web of Science ®Google Scholar
• COLETT A, HIGGS NB, SIMS E et al.: Modulation of the permeability of H2 receptor antagonists cimetidine and ranitidine by P-glycoprotein in rat intestine and the human colonic cell line Caco-2. J. Pharmacol. Exp. Ther. (1999) 288:171–178.
   PubMed Web of Science ®Google Scholar
• HUANG L, HOFFMAN T, VORE M: Adenosine triphosphate-dependent transport of estradiol-17β-(β-Dglucuronide) in membrane vesicles by MDR1 expressed insect cells. Hepatology (1998) 28:1371–1377.
   PubMed Web of Science ®Google Scholar
• POHL A, DEVAUX PF, HERRMANN A: Function of prokaryotic and eukaryotic ABC proteins in lipid transport. Biochim. Biophys. Acta (2005) 1733:29–52.
   PubMed Web of Science ®Google Scholar
• HAIMEUR A, CONSEIL G, DEELEY RG, COLE SP: The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr. Drug Metab. (2004) 5:21–53.
   PubMed Web of Science ®Google Scholar
• HOPPER E, BELINSKY MG, ZENG H, TOSOLINI A, TESTA JR, KRUH GD: Analysis of the structure and expression pattern of MRP7 (ABCC10), a new member of the MRP subfamily. Cancer Lett. (2001) 162:181–191.
   PubMed Web of Science ®Google Scholar
• GUO Y, KOTOVA E, CHEN ZS et al.: MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2’,3’-dideoxycytidine and 9’-(2’-phosphonylmethoxyethyl)adenine. J. Biol. Chem. (2003) 278:29509–29514.
   PubMed Web of Science ®Google Scholar
• BERA TK, IAVARONE C, KUMAR V, LEE S, LEE B, PASTAN I: MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc. Natl. Acad. Sci. USA (2002) 99:6997–7002.
   PubMed Web of Science ®Google Scholar
• KEPPLER D, KONIG J: Expression and localization of the conjugate export pump encoded by the MRP2 (cMRP/cMOAT) gene in liver. FASEB J. (1997) 11:509–516.
   PubMed Web of Science ®Google Scholar
• CHEN ZS, KAWABE T, ONO M et al.: Effect of multidrug resistance-reversing agents on transporting activity of human canalicular multispecific organic anion transporter. Mol. Pharmacol. (1999) 56(6):1219–1228.
   PubMed Web of Science ®Google Scholar
• CUI Y, KONIG J, BUCHHOLZ JK, SPRING H, LEIER I, KEPPLER D: Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. (1999) 55(5):929–937.
   PubMed Web of Science ®Google Scholar
• EVERS R, KOOL M, VAN DEEMTER L et al.: Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J. Clin. Invest. (1998) 101(7):1310–1319.
   PubMed Web of Science ®Google Scholar
• BORST P, ZELCER N, VAN HELVOORT A: ABC transporters in lipid transport. Biochim. Biophys. Acta. (2000) 1486(1):128–144.
   PubMed Web of Science ®Google Scholar
• RENES J, VRIES GE, JANSEN LM, MULLER M: The (patho) physiological functions of the MRP family. Drug Resist. Updat. (2000) 3:289–302.
   PubMed Web of Science ®Google Scholar
• CNUBBEN NHP, ROMMENS AJ, OUDSHOORN MJ, VAN BLADEREN PJ: Glutathionedependent biotransformation of the alkylating drug thiotepa and transport of its metabolite monoglutathionylthiotepa in human MCF-7 breast cancer cells. Cancer Res. (1998) 58:4616–4623.
   PubMed Web of Science ®Google Scholar
• CNUBBEN NHP, RIETJENS IMCM, WORTELBOER H, VAN ZANDEN J, VAN BLADEREN PJ: The interplay of glutathione-related processes in antioxidant defense. Environ. Toxicol. Pharmacol. (2001) 10:141–152.
   PubMed Web of Science ®Google Scholar
• MORROW CS, SMITHERMAN PK, DIAH SK, SCHNEIDER E, TOWNSEND AJ: 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. (1998) 273:20114–20120.
   PubMed Web of Science ®Google Scholar
• MORROW CS, SMITHERMAN PK, TOWNSEND AJ: Combined expression of multidrug resistance protein (MRP) and glutathione S-transferase P1–1 (GSTP1–1) in MCF7 cells and high level resistance to the cytotoxicities of ethacrynic acid but not oxazaphosphorines or cisplatin. Biochem. Pharmacol. (1998) 56:1013–1021.
   PubMed Web of Science ®Google Scholar
• TEODORI E, DEI S, SCAPECCHI S, GUALTIERI F: The medicinal chemistry of multidrug resistance (MDR) reversing drugs. Farmaco (2002) 57(5):385–415.
   PubMedGoogle Scholar
• SAWICKA M, KALINOWSKA M, SKIERSKI J, LEWANDOWSKI W: A review of selected anti-tumour therapeutic agents and reasons for multidrug resistance occurrence. J. Pharm. Pharmacol. (2004) 56:1067–1081.
   PubMed Web of Science ®Google Scholar
• GARRAWAY LA, CHABNER B: MDR1 inhibition: less resistance or less relevance? Eur. J. Cancer (2002) 38:2337–2340.
   PubMed Web of Science ®Google Scholar
• LEONESSA F, CLARKE R: ATP binding cassette transporters and drug resistance in breast cancer. Endocr. Relat. Cancer (2003) 10:43–73.
   PubMed Web of Science ®Google Scholar
• SPARREBOOM A, DANESI R, ANDO Y, CHAN J, FIGG WD: Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Res. Updat. (2003) 10:71–84.
   Google Scholar
• O’BRIEN ML, TEW KD: Glutathione and related enzymes in multidrug resistance. Eur. J. Cancer (1996) 32A(6):967–978.
   PubMed Web of Science ®Google Scholar
• SARKADI B, OZVEGY-LACZKA C, NEMET K, VARADI A: ABCG2. a transporter for all seasons. FEBS Letters (2004) 567:116–120.
   PubMed Web of Science ®Google Scholar
• KRUH GD, BELINSKY MG: The MRP family of drug efflux pumps. Oncogene (2003) 22(47):7537–7552.
   PubMed Web of Science ®Google Scholar
• LOE DW, ALMQUIST KC, DEELEY RG, COLE SP: Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J. Biol. Chem. (1996) 271(16):9675–9682.
   PubMed Web of Science ®Google Scholar
• LOE DW, DEELEY RG, COLE SP: Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res. (1998) 58:5130–5136.
   PubMed Web of Science ®Google Scholar
• RAPPA G, LORICO A, FLAVELL RA, SARTORELLI AC: Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. (1997) 57:5232–5237.
   PubMed Web of Science ®Google Scholar
• SAKAMOTO H, HARA H, HIRANO K, ADACHI T: Enhancement of glucuronosyl etoposide transport by glutathione in multidrug resistance-associated proteinoverexpressing cells. Cancer Lett. (1999) 135:113–119.
   PubMed Web of Science ®Google Scholar
• QIAN YM, SONG WC, CUI H, COLE SP, DEELEY RG: Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J. Biol. Chem. (2001) 276:6404–6411.
   PubMed Web of Science ®Google Scholar
• LESLIE EM, ITO K, UPADHYAYA P, HECHT SS, DEELEY RG, COLE SP: 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. (2001) 276:27846–27854.
   PubMed Web of Science ®Google Scholar
• LESLIE EM, DEELEY RG, COLE SP: Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab. Dispos. (2003) 31(1):11–15.
   PubMed Web of Science ®Google Scholar
• LOE DW, DEELEY RG, COLE SP: Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J. Pharmacol. Exp. Ther. (2000) 293(2):530–538.
   PubMed Web of Science ®Google Scholar
• KÖNIG J, NIES AT, CUI Y, LEIR I, KEPPLER D: Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity and MRP2-mediated drug resistance. Biochim. Biophys. Acta (1999) 1461:377–394.
   PubMed Web of Science ®Google Scholar
• BAKOS E, EVERS R, SINKO E, VARADI A, BORST P, SARKADI B: Interaction of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. (2000) 57:760–768.
   PubMed Web of Science ®Google Scholar
• NIES AT, KÖNIG J, CUI Y, BROM M, SPRING H, KEPPLER D: Structural requirements for the apical sorting of human multidrug resistance protein 2 (ABCC2). Eur. J. Biochem. (2002) 269:1886–1876.
   PubMedGoogle Scholar
• KOIKE K, KAWABE T, TANAKA T et al.: A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res. (1997) 57(24):5475–5479.
   PubMed Web of Science ®Google Scholar
• HOOIJBERG JH, BROXTERMAN HJ, KOOL M et al.: Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res. (1999) 59(11):2532–2535.
   PubMed Web of Science ®Google Scholar
• DOYLE LA, YANG W, ABRUZZO LV et al. : A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA (1998) 95(26):15665–15670.
   PubMed Web of Science ®Google Scholar
• XU J, LIU Y, YANG Y, BATES S, ZHANG JT: Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J. Biol. Chem. (2004) 279:19781–19789.
   PubMed Web of Science ®Google Scholar
• LESLIE EM, DEELEY RG, COLE SPC: Multidrug resistance proteins: role of Pglycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. (2005) 204:216–237.
   PubMed Web of Science ®Google Scholar
• DOYLE LA, ROSS DD: Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene (2003) 22:7340–7358.
   PubMed Web of Science ®Google Scholar
• JANVILISRI T, VENTER H, SHAHI S et al.: Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in lactococcus lactis. J. Biol. Chem. (2003) 278:20645–20651.
   Google Scholar
• NAKANISHI T, DOYLE LA, HASSEL B et al.: Functional characterization of human breast cancer resistance protein (BCRP, ABCG2) expressed in the oocytes of Xenopus laevis. Mol. Pharmacol. (2003) 64:1452–1462.
   Google Scholar
• ROBEY RW, MEDINA-PEREZ WY, NISHIYAMA K et al.: Overexpression of the ATP-binding cassette half-transporter, ABCG2 (MXR/BCRP/ABCP1), in flavopiridol resistant human breast cancer cells. Clin. Cancer Res. (2001) 7:145–152.
   PubMed Web of Science ®Google Scholar
• IMAI Y, ASADA S, TSUKAHARA S et al.: Breast cancer resistance protein exports sulfated estrogens but not free estrogens. Mol. Pharmacol. (2003) 64:610–618.
   PubMed Web of Science ®Google Scholar
• COORAY HC, JANVILISRI T, VAN VEEN HW, HLADKY SB, BARRAND MA: Interaction of the breast cancer resistance protein with plant polyphenols. Biochem. Biophys. Res. Commun. (2004) 317:269–275.
   PubMed Web of Science ®Google Scholar
• SERRANO MA, BAYON JE, PASCOLO L et al. Evidence for carrier-mediated transport of unconjugated bilirubin across plasma membrane vesicles from human placental trophoblast. Placenta (2002) 23:527–535.
   PubMed Web of Science ®Google Scholar
• HOFFMANN U, KROEMER HK: The ABC transporters MDR1 and MRP2: multiple functions in disposition of xenobiotics and drug resistance. Drug Metab. Rev. (2004) 36:669–701.
   PubMed Web of Science ®Google Scholar
• FRANKS ME, MACPHERSON GR, LEPPER ER, FIGG WD, SPARREBOOM A: New directions in cancer research: technological advances in biology, drug resistance, and molecular pharmacology. Drug Resist. Updat. (2003) 6:301–312.
   PubMed Web of Science ®Google Scholar
• KRISHNA R, MAYER LD: Multidrug resistance (MDR) in cancer, mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur. J. Pharm. Sci. (2000) 11:265–283.
   PubMed Web of Science ®Google Scholar
• LEONARD GD, FOJO T, BATES SE: The role of ABC transporters in clinical practice. The Oncologist (2003) 8:411–424.
   PubMed Web of Science ®Google Scholar
• KRUIJTZER CMF, BEIJNEN JH, SCHELLENS JHM: Improvement of oral drug treatment by temporary inhibition of drug transporters and/or cytochrome P450 in the gastrointestinal tract and liver: an overview. The Oncologist (2002) 7:516–530.
   PubMed Web of Science ®Google Scholar
• BODO A, BAKOS E, SZERI F, VÁRADI A, SARKADI B: The role of multidrug transporters in drug availability, metabolism and toxicity. Toxicol. Lett. (2003) 140–141:133–143.
   Google Scholar
• SHTIL AA: Signal transduction pathways and transcriptional mechanisms as targets for prevention of emergence of multidrug resistance in human cancer cells. Curr. Drug Targets (2001) 2:57–77.
   PubMed Web of Science ®Google Scholar
• NIETH C, PRIEBSCH A, STEGE A, LAGE H: Modulation of the classical multidrug resistance (MDR) phenotype by RNA interference (RNAi). FEBS Letters (2003) 545:144–150.
   PubMed Web of Science ®Google Scholar
• OSADA H, TOKUNAGA T, ABE Y et al.: Reversal of drug resistance mediated by hammerhead ribozyme against multidrug resistance-associated protein 1 in a human glioma cell line. Int. J. Oncol. (2003) 22(4):823–827.
   PubMed Web of Science ®Google Scholar
• NAGATA J, KIJIMA H, HATANAKA H et al.: Reversal of drug resistance using hammerhead ribozymes against multidrug resistance-associated protein and multidrug resistance 1 gene. Int. J. Oncol. (2002) 21(5):1021–1026.
   PubMed Web of Science ®Google Scholar
• PEASTON AE, GARDANEH M, FRANCO AV et al. : MRP1 gene expression level regulates the death and differentiation response of neuroblastoma cells. Br. J. Cancer (2001) 85(10):1564–1571.
   PubMed Web of Science ®Google Scholar
• STEWART AJ, CANITROT Y, BARACCHINI E, DEAN NM, DEELEY RG, COLE SP: Reduction of expression of the multidrug resistance protein (MRP) in human tumor cells by antisense phosphorothioate oligonucleotides. Biochem. Pharmacol. (1996) 51(4):461–469.
   PubMed Web of Science ®Google Scholar
• KOIKE K, KAWABE T, TANAKA T et al.: A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res. (1997) 57(24):5475–5479.
   PubMed Web of Science ®Google Scholar
• EE PLR, HE X, ROSS DD, BECK WT: Modulation of breast cancer resistance protein (BCRP/ABCG2) gene expression using RNA interference. Mol. Cancer Ther. (2004) 3:1577–1584.
   PubMed Web of Science ®Google Scholar
• SPARREBOOM A, NOOTER K: Does P-glycoprotein play a role in anticancer drug pharmacokinetics. Drug Resist. Updat. (2000) 3:357–363.
   PubMed Web of Science ®Google Scholar
• HEDEGUS T, ORFI L, SEPRODI A, VARADI A, SARKADI B, KERI G: Interaction of tyrosine kinase inhibitors with the human multidrug transporter proteins, MDR1 and MRP1. Biochim. Biophys. Acta. - Molecular Basis of Disease (2002) 1578(2–3):318–325.
   Google Scholar
• GEKELER V, ISE W, SANDERS KH, ULRICH WR, BECK J: The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. (1995) 208(1):345–352.
   PubMed Web of Science ®Google Scholar
• TOUHEY S, O’CONNOR R, PLUNKETT S, MAGUIRE A, CLYNES M: Structure-activity relationship of indomethacin analogues for MRP-1, COX-1 and COX-2 inhibition: identification of novel chemotherapeutic drug resistance modulators. Eur. J. Cancer (2002) 38:1661–1670.
   PubMed Web of Science ®Google Scholar
• PRIME CHAPMAN HM, FEARN RA, COOPER AE, MOORE V, HIRST BH: Differential multidrug-resistance associated protein 1 through 6 isoform expression and function in human intestinal epithelial Caco-2 cells. J. Pharmacol. Exp. Ther. (2004) 311:476–484.
   PubMed Web of Science ®Google Scholar
• LOE DW, OLESCHUK CJ, DEELEY RG, COLE SPC: Structure-activity studies of verapamil analogs that modulate transport of leucotriene C4 and reduced glutathione by multidrug resistance protein MRP1. Biochem. Biophys. Res. Commun. (2000) 275:795–803.
   PubMed Web of Science ®Google Scholar
• KIM HS, MIN YD, CHOI CH: Doubleedged sword of chemosensitizer: increase of multidrug resistance protein (MRP) in leukemic cells by an MRP inhibitor probenecid. Biochem. Biophys. Res. Commun. (2001) 283(1):64–71.
   PubMed Web of Science ®Google Scholar
• GOLLAPUDI S, KIM CH, TRAN BN, SANGHA S, GUPTA S: Probenecid reverses multidrug resistance in multidrug resistance-associated protein-overexpressing HL60/AR and H69/AR cells but not in P-glycoprotein-overexpressing HL60/Tax and P388/ADR cells. Cancer Chemother. Pharmacol. (1997) 40(2):150–158.
   PubMed Web of Science ®Google Scholar
• DRAPER MP, MARTELL RL, LEVY SB: Indomethacin-mediated reversal of multidrug resistance and drug efflux in human and murine cell lines overexpressing MRP, but not P-glycoprotein. Br. J. Cancer (1997) 75(6):810–815.
   PubMed Web of Science ®Google Scholar
• BAKOS E, EVERS R, SINKO E, VARADI A, BORST P, SARKADI B: Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. (2000) 57(4):760–768.
   PubMed Web of Science ®Google Scholar
• GERMANN UA, SHLYAKHTER D, MASON VERSUS et al.: Cellular and biochemical characterization of VX-710 as a chemosensitizer: reversal of P-glycoproteinmediated multidrug resistance in vitro. Anti-Cancer Drugs (1997) 8(2):125–140.
   Google Scholar
• GERMANN UA, FORD PJ, SHLYAKHTER D, MASON VS, HARDING MW: Chemosensitization and drug accumulation effects of VX-710, verapamil, cyclosporin A, MS-209 and GF120918 in multidrug resistant HL60/ ADR cells expressing the multidrug resistance-associated protein MRP. Anti-cancer Drugs (1997) 8(2):141–155.
   PubMed Web of Science ®Google Scholar
• AOKI S, CHEN ZS, HIGASIYAMA K, SETIAWAN A, AKIYAMA S, KOBAYASHI M: Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn. J. Cancer Res. (2001) 92(8):886–895.
   PubMedGoogle Scholar
• SUMIZAWA T, CHEN ZS, CHUMAN Y et al.: Reversal of multidrug resistanceassociated protein-mediated drug resistance by the pyridine analog PAK-104P. Mol. Pharmacol. (1997) 51(3):399–405.
   PubMed Web of Science ®Google Scholar
• MARBEUF-GUEYE C, SALERNO M, QUIDU P, GARNIER-SUILLEROT A: Inhibition of the P-glycoprotein- and multidrug resistance protein-mediated efflux of anthracyclines and calceinacetoxymethyl ester by PAK-104P. Eur. J. Pharmacol. (2000) 391(3):207–216.
   PubMed Web of Science ®Google Scholar
• BARRAND MA, RHODES T, CENTER MS, TWENTYMAN PR: Chemosensitisation and drug accumulation effects of cyclosporin A, PSC-833 and verapamil in human MDR large cell lung cancer cells expressing a 190k membrane protein distinct from P-glycoprotein. Eur. J. Cancer (1993) 29A(3):408–415.
   Web of Science ®Google Scholar
• HOOIJBERG JH, BROXTERMAN HJ, SCHEFFER GL et al. : Potent interaction of flavopiridol with MRP1. Br. J. Cancer (1999) 81(2):269–276.
   PubMed Web of Science ®Google Scholar
• VERSANTVOORT CH, RHODES T, TWENTYMAN PR: Acceleration of MRPassociated efflux of rhodamine 123 by genistein and related compounds. Br. J. Cancer (1996) 74(12):1949–1954.
   PubMed Web of Science ®Google Scholar
• NGUYEN H, ZHANG S, MORRIS ME: Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J. Pharm. Sci. (2003) 92(2):250–257.
   PubMed Web of Science ®Google Scholar
• LESLIE EM, MAO Q, OLESCHUK CJ, DEELEY RG, COLE SP: Modulation of multidrug resistance protein 1 (MRP1/ ABCC1) transport and ATP-ase activities by interaction with dietary flavonoids. Mol. Pharmacol. (2001) 59(5):1171–1180.
   PubMed Web of Science ®Google Scholar
• BANDI N, KOMPELLA UB: Budesonide reduces multidrug resistance-associated protein 1 expression in an airway epithelial cell line (Calu-1). Eur. J. Pharmacol. (2002) 437(1–2):9–17.
   Google Scholar
• PAYEN L, DELUGIN L, COURTOIS A, TRINQUART Y, GUILLOUZO A, FARDEL O: Reversal of MRP-mediated multidrug resistance in human lung cancer cells by the antiprogestatin drug RU486. Biochem. Biophys. Res. Commun. (1999) 258(3):513–518.
   PubMed Web of Science ®Google Scholar
• NAKANO R, OKA M, NAKAMURA T et al.: A leukotriene receptor antagonist, ONO-1078, modulates drug sensitivity and leukotriene C4 efflux in lung cancer cells expressing multidrug resistance protein. Biochem. Biophys. Res. Commun. (1998) 251(1):307–312.
   PubMed Web of Science ®Google Scholar
• PAYEN L, DELUGIN L, COURTOIS A, TRINQUART Y, GUILLOUZO A, FARDEL O: The sulphonylurea glibenclamide inhibits multidrug resistance protein (MRP1) activity in human lung cancer cells. Br. J. Pharmacol. (2001) 132(3):778–784.
   PubMed Web of Science ®Google Scholar
• NORMAN BH: Inhibitors of MRP1- mediated multidrug resistance. Drugs of the future (1998) 23:1001–1013.
   Google Scholar
• BURG D, WIELINGA P, ZELCER N, SAEKI T, MULDER GJ, BORST P: Inhibition of the multidrug resistance protein 1 (MRP1) by peptidomimetic glutathione-conjugate analogs. Mol. Pharmacol. (2002) 62(5):1160–1166.
   PubMed Web of Science ®Google Scholar
• NORMAN BH, GRUBER JM, HOLLINSHEAD SP et al. : Tricyclic isoxazoles are novel inhibitors of the multidrug resistance protein (MRP1). Bioorg. Med. Chem. Lett. (2002) 12(6):883–886.
   Google Scholar
• QIAN YM, GRANT CE, WESTLAKE CJ et al. : Photolabeling of human and murine multidrug resistance protein 1 with the high affinity inhibitor [125I]LY475776 and azidophenacyl- [35S]glutathione. J. Biol. Chem. (2002) 277(38):35225–35231.
   PubMed Web of Science ®Google Scholar
• VAN LOEVEZIJN A, ALLEN JD, SCHINKEL AH, KOOMEN GJ: Inhibition of BCRP-mediated drug efflux by fumitremorgin-type indolyl diketopiperazines. Bioorg. Med. Chem. Lett. (2001) 11:29–32.
   PubMed Web of Science ®Google Scholar
• DE BRUIN M, MIYAKE K, LITMAN T, ROBEY R, BATES SE: Reversal of resistance by GF120918 in cell lines expressing the ABC-half transporter, MXR. Cancer Lett. (1999) 146:117–126.
   PubMed Web of Science ®Google Scholar
• EVERS R, KOOL M, SMITH AJ, VAN DEEMTER L, DE HAAS M, BORST P: Inhibitory effect of the reversal agents V-104, GF120918 and pluronic L61 on MDR1 Pgp, MRP1 and MRP2 mediated transport. Br. J. Cancer (2002) 83:366–374.
   Web of Science ®Google Scholar
• BAKOS E, EVERS R, SZAKACS G et al.: Functional multidrug resistance (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem. (1998) 273:32167–32175.
   PubMed Web of Science ®Google Scholar
• WORTELBOER HM, USTA M, VAN DER VELDE AE et al.: Interplay between MRP inhibition and metabolism of MRP inhibitors: the case of curcumin. Chem. Res. Toxicol. (2003) 16:1642–1651.
   PubMed Web of Science ®Google Scholar
• VAN ZANDEN JJ, WORTELBOER HM, BIJLSMA S et al.: Quantitative structure activity relationship studies on the flavonoid mediated inhibition of multidrug resistance proteins MRP1 and 2. Biochem. Pharmacol. (2005) 69:699–708.
   PubMed Web of Science ®Google Scholar
• PAVEK P, MERINO G, WAGENAAR E et al.: Human breast cancer resistance protein (BCRP/ABCG2): interactions with steroid drugs, hormones, the dietary carcinogen PhIP, and transport of cimetidine. J. Pharmacol. Exp. Ther. (2004) 312:144–152.
   PubMed Web of Science ®Google Scholar
• BAKOS E, EVERS R, SZAKACS G et al.: Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem. (1998) 273:32167–32175.
   PubMed Web of Science ®Google Scholar
• URBATSCH IL, SANKARAN B, WEBER J, SENIOR AE: P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. (1995) 270:19383–19390.
   PubMed Web of Science ®Google Scholar
• BUXBAUM E: Co-operative binding sites for transported substrates in the multiple drug resistance transporter Mdr1. Eur. J. Biochem. (1999) 265:64–70.
   PubMedGoogle Scholar
• RAPPA G, LORICO A, HILDINGER M, FODSTAD O, BAUM C: Novel bicistronic retroviral vector expressing gammaglutamylcysteine synthetase and the multidrug resistance protein 1 (MRP1) protects cells from MRP1-effluxed drugs and alkylating agents. Hum. Gene Ther. (2001) 12:1785–1796.
   PubMed Web of Science ®Google Scholar
• TOWNSEND DM, TEW KD: The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene (2003) 22(47):7369–7375.
   PubMed Web of Science ®Google Scholar
• VAN BLADEREN PJ, VAN OMMEN B: The inhibition of glutathione S-transferases: mechanisms, toxic consequences and therapeutic benefits. Pharmacol. Ther. (1991) 51(1):35–46.
   PubMed Web of Science ®Google Scholar
• SHEN H, KAUVAR L, TEW KD: Importance of glutathione and associated enzymes in drug response. Oncol. Res. (1997) 9(6–7):295–302.
   Google Scholar
• GATE L, TEW KD: Glutathione Stransferases as emerging therapeutic targets. Expert Opin. Ther. Targets (2001) 5(4):477–489.
   PubMedGoogle Scholar
• TEW KD, DUTTA S, SCHULTZ M: Inhibitors of glutathione S-transferases as therapeutic agents. Adv. Drug Deliv. Rev. (1997) 26(2–3):91–104.
   Google Scholar
• TURCOTTE S, AVERILL-BATES DA: Sensitization to the cytotoxicity of melphalan by ethacrynic acid and hyperthermia in drug-sensitive and multidrug-resistant Chinese hamster ovary cells. Radiat. Res. (2001) 156(3):272–282.
   PubMed Web of Science ®Google Scholar
• HAMILTON D, FOTOUHI-ARDAKANI N, BATIST G: The glutathione system in alkylator resistance. Cancer Treat. Res. (2002) 112:67–87.
   PubMedGoogle Scholar
• VAN DER WOUDE H, BOERSMA MG, VERVOORT J, RIETJENS IMCM: Identification of 14 quercetin Phase II mono- and mixed conjugates and their formation by rat and human Phase II in vitro model systems. Chem. Res. Toxicol. (2004) 17:1520–1530.
   PubMed Web of Science ®Google Scholar
• WORTELBOER HM, USTA M, VAN ZANDEN JJ, VAN BLADEREN PJ, RIETJENS IMCM, CNUBBEN NHP: Inhibition of multidrug resistance proteins MRP1 and MRP2 by a series of α,β- unsaturated carbonyl compounds. Biochem. Pharmacol. (2005) 69:1879–1890.
   PubMed Web of Science ®Google Scholar
• ZAMAN GJR, CNUBBEN NHP, VAN BLADEREN PJ, EVERS R, BORST P: Transport of the glutathione conjugate of ethacrynic acid by the human multidrug resistance protein MRP. FEBS Lett. (1996) 391:126–130.
   PubMed Web of Science ®Google Scholar
• VAN IERSEL ML, PLOEMEN JHTM, STRUIK I et al.: Inhibition of glutathione S-transferase activity in human melanoma cells by α,β-unsaturated carbonyl derivatives. Effects of acrolein, cinnamaldehyde, citral, crotonaldehyde, curcumin, ethacrynic acid and trans-2- hexenal. Chem. Biol. Interact. (1996) 102:117–132.
   PubMed Web of Science ®Google Scholar
• BOGAARDS JJP, VENEKAMP JC, VAN BLADEREN PJ: Stereoselective conjugation of prostaglandin A2 and prostaglandin J2 with glutathione, catalyzed by the human glutathione S-transferases. Chem. Res. Tox. (1997) 10:310–317.
   PubMed Web of Science ®Google Scholar
• EVERS R, CNUBBEN NHP, WIJNHOLDS J, VAN DEEMTER L, VAN BLADEREN PJ, BORST P: Transport of glutathione prostaglandin A conjugates by the multidrug resistance protein 1. FEBS Lett. (1997) 419:112–116.
   PubMed Web of Science ®Google Scholar
• VAN IERSEL ML, CNUBBEN NHP, SMINK N, KOEMAN JH, VAN BLADEREN PJ: Interactions of prostaglandin A2 with the glutathionemediated biotransformation system. Biochem. Pharmacol. (1999) 57(12):1383–1390.
   PubMed Web of Science ®Google Scholar
• NIJVELDT RJ, VAN NOOD E, VAN HOORN DE, BOELENS PG, VAN NORREN K, VAN LEEUWEN PA: Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. (2001) 74(4):418–425.
   PubMed Web of Science ®Google Scholar
• ZHANG K, DAS NP: Inhibitory effects of plant polyphenols on rat liver glutathione S transferases. Biochem. Pharmacol. (1994) 47:2063–2068.
   PubMed Web of Science ®Google Scholar
• VAN ZANDEN JJ, BEN HAMMAN O, VAN IERSEL MLPS et al.: Inhibition of human glutathione S-transferase P1–1 by the flavonoid quercetin. Chem. Biol. Interact. (2003) 145(2):139–148.
   PubMed Web of Science ®Google Scholar
• HOOIJBERG JH, BROXTERMAN HJ, HEIJN M, FLES DL, LANKELMA J, PINEDO HM: Modulation by (iso)flavonoids of the ATPase activity of the multidrug resistance protein. FEBS Lett. (1997) 413(2):344–348.
   PubMed Web of Science ®Google Scholar
• LESLIE EM, MAO Q, OLESCHUK CJ, DEELEY RG, COLE SP: Modulation of multidrug resistance protein 1 (MRP1/ ABCC1) transport and atpase activities by interaction with dietary flavonoids. Mol. Pharmacol. (2001) 59(5):1171–1180.
   PubMed Web of Science ®Google Scholar
• ZHANG S, YANG X, MORRIS ME: Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Mol. Pharmacol. (2004) 65(5):1208–1216.
   PubMed Web of Science ®Google Scholar
• IMAI Y, TSUKAHARA S, ASADA S, SUGIMOTO Y: Phytoestrogens/flavonoids reverse breast cancer resistance protein/ ABCG2-mediated multidrug resistance. Cancer Res. (2004) 64(12):4346–4352.
   PubMed Web of Science ®Google Scholar
• DI PIETRO A, CONSEIL G, PEREZ-VICTORIA JM et al. : Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell Mol. Life Sci. (2002) 59(2):307–322.
   Google Scholar
• HAYSTEEN BH: The biochemistry and medical significance of the flavonoids. Pharmacol. Ther. (2002) 96(2–3):67–202.
   Google Scholar
• WILLIAMS RJ, SPENCER JP, RICE-EVANS C: Flavonoids: antioxidants or signalling molecules? Free Radic. Biol. Med. (2004) 36:838–849.
   Google Scholar
• RODGERS EH, GRANT MH: The effect of the flavonoids, quercetin, myricetin and epicatechin on the growth and enzyme activities of MCF7 human breast cancer cells. Chem. Biol. Interact. (1998) 116:213–228.
   PubMed Web of Science ®Google Scholar
• GALATI G, O’fBRIEN PJ: Potential toxicity of flavonoids and other dietary phenolics: significance for their chemopreventive and anticancer properties. Free Radic. Biol. Med. (2004) 37(3):287–303.
   PubMed Web of Science ®Google Scholar
• GRAEFE EU, DERENDORF H, VEIT M: Pharmacokinetics and bioavailability of the flavonol quercetin in humans. Int. J. Clin. Pharmacol. Ther. (1999) 37(5):219–233.
   PubMed Web of Science ®Google Scholar
• HOLLMAN PC, VD GAAG M, MENGELERS MJ, VAN TRIJP JM, DE VRIES JH, KATAN MB: Absorption and disposition kinetics of the dietary antioxidant quercetin in man. Free Radic. Biol. Med. (1996) 21(5):703–707.
   PubMed Web of Science ®Google Scholar
• BAGRIJ T, KLOKOUZAS A, HLADKY SB, BARRAND MA: Influences of glutathione on anionic substrate efflux in tumour cells expressing the multidrug resistance-associated protein, MRP1. Biochem. Pharmacol. (2001) 62(2):199–206.
   PubMed Web of Science ®Google Scholar
• WALLE UK, GALIJATOVIC A, WALLE T: Transport of the flavonoid chrysin and its conjugated metabolites by the human intestinal cell line Caco-2. Biochem. Pharmacol. (1999) 58(3):431–438.
   PubMed Web of Science ®Google Scholar
• WALGREN RA, KARNAKY KJ Jr, LINDENMAYER GE, WALLE T: Efflux of dietary flavonoid quercetin 4’-betaglucoside across human intestinal Caco-2 cell monolayers by apical multidrug resistance- associated protein-2. J. Pharmacol. Exp. Ther. (2000) 294(3):830–836.
   PubMed Web of Science ®Google Scholar
• DAY A, MELLON F, BARRON D, SARRAZIN G, MORGAN MR, WILLIAMSON G: Human metabolism of dietary flavonoids: Identification of plasma metabolites of quercetin. Free Radic. Res. (2001) 35:941–952.
   PubMed Web of Science ®Google Scholar
• MORAND C, CRESPY V, MANACH C, BESSON C, DEMIGNE C, REMESY C: Plasma metabolites of quercetin and their antioxidant properties. Am. J. Physiol. (1998) 275:R212–R219.
   PubMed Web of Science ®Google Scholar
• TROMPIER D, BAUBICHON-CORTAY H, CHANG XB et al.: Multiple flavonoid-binding sites within multidrug resistance protein MRP1. Cell Mol. Life Sci. (2003) 60(10):2164–2177.
   PubMed Web of Science ®Google Scholar