Inhibitory effect of the reversal agents V-104, GF120918 and pluronic L61 on MDR1 Pgp-, MRP1- and MRP2-mediated transport

British Journal of Cancer

Volumn 83, Issue 3, 2000, Pages 366-374

  Evers, R ^a,b   Kool, M ^a,c   Smith, A J ^a,c   Van Deemter, L ^a   De Haas, M ^a   Borst, P ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

MDR1 Pgp; MRP1; Multidrug resistance; Multispecific organic anion transporter; Polarized cell; Reversal agent

Indexed keywords

2 BROMOMETHAMPHETAMINE; CALCEIN; COMPLEMENTARY DNA; DAUNORUBICIN; ELACRIDAR; ETOPOSIDE; GLUTATHIONE DERIVATIVE; MULTIDRUG RESISTANCE PROTEIN; POLOXAMER; UNCLASSIFIED DRUG; VINBLASTINE;

ANIMAL CELL; ARTICLE; CANCER CELL; DRUG TRANSPORT; MULTIDRUG RESISTANCE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL;

EID: 0033922511     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1054/bjoc.2000.1260     Document Type: Article

References (48)

1. Bakos E, Evers R, Szakacs G, Tusnad, GE, Welker E, Szabo K, de Haas M, van Deemter L, Borst P, Varadi A and Sarkadi B (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273: 32167-32175
2. Batrakova EV, Han HY, Miller DW and Kabanov AV (1998) Effects of pluronic P85 unimers and micelles on drug permeability in polarized BBMEC and Caco-2 cells. Pharm Res 15: 1525-1532
3. Batrakova EV, Dorodnych TY, Klinskii EY, Kliushnenkova EN, Hemchukova OB, Goncharova ON, Arjakov SA, Alakhov VY and Kabanov AV (1996) Anthracycline antibiotics non-covalently incorporated into the block copolymer micelles: in vivo evaluation of anti-cancer activity. Br J Cancer 74: 1545-1552
4. Böhme M, Büchler M., Müller M and Keppler D (1993) Differential inhibition of cyclosporins of primary-active ATP-dependent transporters in the hepatocyte canalicular membrane. FEBS Lett 333: 193-196
5. Chen ZS, Kawabe T, Ono M, Aoki S, Sumizawa T, Furukawa T, Uchiumi T, Wada M, Kuwano M and Akiyama SI (1999) Effect of multidrug resistance-reversing agents on transporting activity of human canalicular multispecific organic anion transporter. Mol Pharmacol 56: 1219-1228
6. Cole SPC and Deeley RG (1998) Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioassays 20: 931-940
7. Cole SPC, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AMV and Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258: 1650-1654
8. Cui Y, König J, Buchholz U, Spring H, Leier I and Keppler D (1999) Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 55: 929-937
9. Evers R, Cnubben WHP, Wijnholds J, van Deemter C, van Bladeren P and Borst P (1997) Transport of glutathione prostaglandin A conjugates by the multidrug resistance protein 1. FEBS Lett 419: 112-116
10. Evers R, de Haas M, Sparidans R, Beijnen J, Wielinga PR, Lankelma L and Borst P (2000) Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br J Cancer 83: 375-383
11. Evers R, Zaman GJR, van Deemter L, Jansen H, Calafat J, Oomen LCJM, Oude Elferink RPJ, Borst P and Schinkel AH (1996) Basolateral localization and export activity of the human multidrug resistance-associated protein in polarized pig kidney cells. J Clin Invest 97: 1211-1218
12. Evers R, Kool M, van Deemeter L, Janssen H, Calafat J, Oomen LCJM, Paulusma CC, Oude Elferink RPJ, Baas F, Schinkel AH and Borst P (1998) Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Invest 101: 1310-1319
13. Feller N, Broxterman HJ, Wähler DCR and Pinedo HM (1995) ATP-dependent efflux of calcein by the multidrug resistance protein (MRP): no inhibition by intracellular glutathione depletion. FEBS Lett 368: 385-388
14. Fisher GA and Sikic BI (1995) Clinical studies with modulators of multidrug resistance. Hematol Oncol Clin North Am 9: 363-382
15. Germann UA, Shlyakhter D, Mason VS, Zelle RE, Duffy JP, Galullo V, Armistead DM, Saunders JO, Boger J and Harding MW (1997a) Cellular and biochemical characterization of VX-710 as a chemosensitizer: reversal of P-glycoprotein-mediated multidrug resistance in vitro. Anticancer Drugs 8: 125-140
16. Germann UA, Ford PJ, Shlyakhter D, Mason VS and Harding MW (1997b) Chemosensitization and drug accumulation effects of VX710, verapamil, cyclosporin A, MS209 and GF120918 in multidrug resistant HL60/ADR cells expressing the multidrug resistance-associated protein MRP. Anticancer Drugs 8: 141-155
17. Gottesmann MM, Hrycyna CA, Schoenlein PV, Germann UA and Pastan I (1995) Genetic analysis of the multidrug transporter. Annu Rev Genet 29: 607-649
18. Hirohashi T, Suzuki H and Sugiyama Y (1999) Characterization of the transport properties of cloned rat multidrug resistance protein 3 (MRP3). J Biol Chem 274: 15181-15185
19. Holló Z, Homolya T, Hegedus T and Sarkadi B (1996) Transport properties of the multidrug resistance-associated protein (MRP) in human tumour cells. FEBS Lett 383: 99-104
20. Homolya L, Holló Z, Müller M, Mechetner EB and Sarkadi B (1996) A new method for a quantitative assessment of P-glycoprotein-related multidrug resistance in tumour cells. Br J Cancer 73: 849-855
21. Hooijberg JH, Broxterman HJ, Kool M, Assaraf YG, Peters GJ, Noordhuis P, Scheper RJ, Borst P, Pinedo HM and Jansen G (1999) Antifolate resistance mediated by the multidrug resistance proteins MRPI and MRP2. Cancer Res 59: 2532-2535
22. Hyafil F, Vergely C, Du Vignaud P and Grand-Perret T (1993) In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxymide derivative. Cancer Res 53: 4595-4602
23. Jedlitschky G, Leier I, Buchholz U, Hummel-Eisenbeiss J, Burchel B and Keppler D (1997) ATP-dependent transport of bilirubin glucuronides by the multidrug resistance protein MRP1 and its hepatocyte canalicular isoform MRP2. Biochem J 327: 305-310
24. Juliano RL and Ling V (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochem Biophys Acta 455: 152-162
25. Keppler D, Jedlitschky G and Leier I (1998) Transport function and substrate specificity of multidrug resistance proteins. Methods Enzymol 292: 607-616
26. Kool M, van der Linden M, de Haas M, Baas F and Borst P (1999a) Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 59: 175-182
27. Kool M, van der Linden M, de Haas M, Scheffer GL, de Vree ML, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, Oude Elferink RPJ, Baas F and Borst P (1999b) MRP3, a new organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 96: 6914-6919
28. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJT, Juijn JA, Baas F and Borst P (1997) Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologs of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res 57: 3527-3547
29. Leier I, Jedlitschky G, Buchholz U, Cole SPC, Deeley RG and Keppler D (1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 269: 27807-27810
30. Loe DW, Almquist KC, Deeley R and Cole SPC (1996) Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. J Biol Chem 271: 9675-9682
31. Loe DW, Deeley RG and Cole SPC (1998) Characterization of vincristine transport by the M(r) 190 000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58: 5130-5136
32. Masuda M, I'izuka Y, Yamazaki M, Nishigaki R, Kato Y, Ni'inuma K, Suzuki H and Sugiyama Y (1998) Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats. Cancer Res 57: 3506-3510
33. Miller DW, Batrakova EV and Kabanov AV (1999) Inhibition of multidrug resistance-associated protein (MRP) functional activity with pluronic block copolymers. Pharmaceutical Res 16: 396-401
34. Miller DW, Batrakova EV, Waltner TO, Alakhov VY and Kabanov AV (1997) Interactions of pluronic block copolymers with brain microvessel endothelial cells: evidence of two potential pathways for drug absorption. Bioconjugate Chem 8: 649-657
35. Müller M, Meijer C, Zaman GJR, Borst P, Scheper RJ, Mulder NH, de Vries EGE and Janssen PLM (1994) Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 91: 8822-8826
36. Nerurkar MM, Ho NFH, Burton PS, Vidmar TJ and Borchardt RT (1997) Mechanistic roles of neutral surfactants on concurrent polarized and passive membrane transport of a model peptide in Caco-2 cells. J Pharm Sci 86: 813-821
37. Oude Elferink RPJ, Bakker CTM and Jansen PLM (1993) Glutathione-conjugate transport by human colon adenocarcinoma cells (Caco-2 cells). Biochem J 290: 759-764
38. Rappa J, Lorico A, Flavell RA and Sartorelli AC (1997) Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 57: 5232-5237
39. Rowinsky EK, Smith L, Wang YM, Chaturvedi P, Villalona M, Campbell E, Aylesworth C, Eckhardt SG, Hammond L, Kraynak M, Drengler R, Stephenson J, Harding MW and Von Hoff DD (1998) Phase I and pharmacokinetic study of paclitaxel in combination with biricodar, a novel agent that reverses multidrug resistance conferred by overexpression of both MDRI and MRP. J Clin Oncol 16: 2964-2967
40. Sarkadi B and Müller M (1997) Search for specific inhibitors of multidrug resistance in cancer. Semin Cancer Biol 8: 171-182
41. Schinkel AH, Wagenaar E, van Deemter L, Mol CAAM and Borst P (1995) Absence of the mdr1a P-glycoprotein in mice affects the tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporin A. J Clin Invest 96: 1698-1705
42. Schuetz JD, Conelly MC, Sun D, Paibir SG, Flynn PM, Srinivas RV, Kumar A and Fridland A (1999) MRP4: A previously unidentified factor in resistance to nucleoside based antiviral drugs. Nat Med 5: 1048-1051
43. Smith AJ, Mayer U, Schinkel AH and Borst P (1998) Availability of PSC833, a substrate and inhibitor of P-glycoprotein, in various concentrations of serum. J Natl Cancer Inst 90: 1161-1166
44. Szabo K, Welker E, Bakos E, Muller M, Roninson I, Varadi A and Sarkadi B (1998) Drug stimulated nucleotide trapping in the human multidrug transporter MDR1. Cooperation of the nucleotide binding domains. J Biol Chem 273: 10132-10138
45. Twentyman PR and Bleehen NM (1991) Resistance modification by PSC833, a novel non-immunosuppressive cyclosporin. Eur J Cancer 27: 1639-1642
46. Venne A, Li S, Mandeville R, Kabanov A and Alakhov V (1996) Hypersensitizing effect of pluronic L61 on cytotoxic activity, transport, and subcellular distribution of doxorubicin in multiple drug-resistant cells. Cancer Res 56: 3626-3629
47. Wallstab A, Koester M, Böhme M and Keppler D (1999) Selective inhibition of MDR1 P-glycoprotein-mediated transport by the acridone carboxamide derivative GG918. Br J Cancer 79: 1053-1060
48. Yanagisawa T, Newman A, Coley H, Renshaw J, Pinkerton CR and Pritchard-Jones K (1999) Biricodar (VX-710; Incel): a selective chemosensitizer in neuroblastoma. Br J Cancer 80: 1190-1196