Multidrug resistance protein 1 (MRP1, ABCC1) mediates resistance to mitoxantrone via glutathione-dependent drug efflux

Molecular Pharmacology

Volumn 69, Issue 4, 2006, Pages 1499-1505

  Morrow, Charles S ^a   Peklak Scott, Christina ^a   Bishwokarma, Bimjhana ^a   Kute, Timothy E ^a   Smitherman, Pamela K ^a   Townsend, Alan J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [[3 [2 (7 CHLOROQUINOLIN 2 YL)VINYL]PHENYL] 2 DIMETHYLCARBAMOYLETHYLSULFANYLMETHYLSULFANYL]PROPIONIC ACID; BREAST CANCER RESISTANCE PROTEIN; GLUTATHIONE; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACCUMULATION; DRUG TRANSPORT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS;

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GLUTATHIONE; HUMANS; MITOXANTRONE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROPIONATES; QUINOLINES;

EID: 33644777840     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.105.017988     Document Type: Article

References (41)

1. Allen JD, Brinkhuis RF, Wijnholds J, and Schinkel AH (1999) The mouse Bcrp1/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res 59:4237-4241.
2. Borst P, Evers R, Kool M, and Wijnholds J (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92:1295-1302.
3. Brangi M, Litman T, Ciotti M, Nishiyama K, Kohlhagen G, Takimoto C, Robey R, Pommier Y, Fojo T, and Bates SE (1999) Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR) and potential for glucuronidation in MXR-expressing cells. Cancer Res 59:5938-5946.
4. Breuninger LM, Paul S, Gaughan K, Miki T, Chan A, Aaronson SA, and Kruh GD (1995) Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res 55:5342-5347.
5. Chu X-Y, Huskey S-EW, Braun MP, Sarkadi B, Evans DC, and Evers R (2004) Transport of ethinylestradiol glucuronide and ethinylestradiol sulfate by the multidrug resistance proteins MRP1, MRP2, and MRP3. J Pharmacol Exp Ther 309:156-164.
6. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, and Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science (Wash DC) 258:1650-1654.
7. Cole SPC, Sparks KE, Fraser K, Loe DW, Grant CE, Wilson GM, and Deeley RG (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54:5902-5910.
8. Consoli U, Van NT, Neamati N, Mahadevia R, Beran M, Zhao S, and Andreeff M (1997) Cellular pharmacology of mitoxantrone in p-glycoprotein-positive and -negative human myeloid leukemic cell lines. Leukemia 11:2066-2074.
9. Dalton WS, Durie BG, Alberts DS, Gerlach JH, and Cress AE (1986) Characterization of a new drug-resistant human myeloma cell line that expresses Pglycoprotein. Cancer Res 46:5125-5130.
10. Diah SK, Smitherman PK, Aldridge J, Volk EL, Schneider E, Townsend AJ, and Morrow CS (2001) Resistance to mitoxantrone in MRP1-expressing MCF7 breast cancer cells: characterization of mitoxantrone transport. Cancer Res 61:5461-5467.
11. Diah SK, Smitherman PK, Townsend AJ, and Morrow CS (1999) Detoxification of 1-chloro-2,4-dinitrobenzene in MCF7 breast cancer cells expressing glutathione S-transferase P1-1 and/or multidrug resistance protein 1. Toxicol Appl Pharmacol 157:85-93.
12. DiPaola RS, Chenven ES, Shih WJ, Lin Y, Amenta P, Goodin S, Shumate A, Capanna T, Cardiella M, Cummings KB, et al. (2001) Mitoxantrone in patients with prostate specific antigen progression after local therapy for prostate carcinoma. Cancer 92:2065-2071.
13. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, and Ross DD (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells [published erratum appears in Proc Natl Acad Sci USA 96:2569]. Proc Natl Acad Sci USA 95:15665-15670.
14. Errington F, Willmore E, Tilby MJ, Li L, Li G, Li W, Baguley BC, and Austin CA (1999) Murine transgenic cells lacking DNA topoisomerase IIβ are resistant to acridines and mitoxantrone: analysis of cytotoxicity and cleavable complex formation. Mol Pharmacol 56:1309-1316.
15. Harker WG, Slade DL, Drake FH, and Parr RL (1991) Mitoxantrone resistance in HL-60 leukemia cells: reduced nuclear topoisomerase II catalytic activity and drug-induced DNA cleavage in association with reduced expression of the topoisomerase II beta isoform. Biochemistry 30:9953-9961.
16. Harker WG, Slade DL, Parr RL, Feldhoff PW, Sullivan DM, and Holguin MH (1995a) Alterations in the topoisomerase II alpha gene, messenger RNA and subcellular protein distribution as well as reduced expression of the DNA topoisomerase II beta enzyme in a mitoxantrone-resistant HL-60 human leukemia cell line. Cancer Res 55:1707-1716.
17. Harker WG, Slade DL, Parr RL, and Holguin MH (1995b) Selective use of an alternative stop codon and polyadenylation signal within intron sequences leads to a truncated topoisomerase II alpha messenger RNA and protein in human HL-60 leukemia cells selected for resistance to mitoxantrone. Cancer Res 55:4962-4971.
18. Kufe DW, Pollock RE, Weichselbaum RR, Bast RC, Gansler TS, Holland JF, and Frei E (2003) Cancer Medicine 6. BC Decker, Inc., Hamilton, ON, Canada.
19. Leslie EM, Deeley RG, and Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2 and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216-237.
20. Leslie EM, Ito K, Upadhyaya P, Hecht SS, Deeley RG, and Cole SPC (2001) Transport of the β-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 276:27846-27854.
21. Litman T, Brangi M, Hudson E, Fetsch P, Abati A, Ross DD, Miyake K, Resau JH, and Bates SE (2000) The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J Cell Sci 113:2011-2021.
22. Loe DW, Almquist KC, Deeley RG, and Cole SPC (1996) Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles: demonstration of glutathione-dependent vincristine transport. J Biol Chem 271:9675-9682.
23. Loe DW, Deeley RG, and Cole SPC (1998) Characterization of vincristine transport by the Mr 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58:5130-5136.
24. Loe DW, Stewart RK, Massey TE, Deeley RG, and Cole SPC (1997) ATP-dependent transport of aflatoxin B1 and its glutathione conjugates by the product of the multidrug resistance protein (MRP) gene. Mol Pharmacol 51:1034-1041.
25. Maliepaard M, van Gastelen MA, de Jong LA, Pluim D, van Waardenburg RC, Ruevekamp-Helmers MC, Floot BG, and Schellens JH (1999) Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res 59:4559-4563.
26. Mirski SE, Gerlach JH, and Cole SP (1987) Multidrug resistance in a human small cell lung cancer cell line selected in adriamycin. Cancer Res 47:2594-2598.
27. Morrow CS, Diah S, Smitherman PK, Schneider E, and Townsend AJ (1998) Multidrug resistance protein and glutathione S-transferase P1-1 act in synergy to confer protection from 4-nitroquinoline 1-oxide toxicity. Carcinogenesis 19:109-115.
28. Nakagawa M, Schneider E, Dixon KH, Horton J, Kelley K, Morrow C, and Cowan KH (1992) Reduced intracellular drug accumulation in the absence of P-glycoprotein (mdr1) overexpression in mitoxantrone-resistant human MCF-7 breast cancer cells. Cancer Res 52:6175-6181.
29. Paumi CM, Ledford BG, Smitherman PK, Townsend AJ, and Morrow CS (2001) Role of multidrug resistance protein 1 (MRP1) and glutathione S-transferase A1-1 in alkylating agent resistance. Kinetics of glutathione conjugate formation and efflux govern differential cellular sensitivity to chlorambucil versus melphalan toxicity. J Biol Chem 276:7952-7956.
30. Peklak-Scott C, Townsend AJ, and Morrow CS (2005) Dynamics of glutathione conjugation and conjugate efflux in detoxification of the carcinogen, 4-nitroquinoline 1-oxide: contributions of glutathione, glutathione S-transferase and MRP1. Biochemistry 44:4426-4433.
31. Qian Y-M, Song W-C, Cui H, Cole SPC, and Deeley RG (2001) Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276:6404-6411.
32. Rappa G, 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.
33. Renes J, De Vries EGE, Nienhuis EF, Jansen PLM, and Müller M (1999) ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br J Pharmacol 126:681-688.
34. Ross DD, Yang W, Abruzzo LV, Dalton WS, Schneider E, Lage H, Dietel M, Greenberger L, Cole SP, and Doyle LA (1999) Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J Natl Cancer Inst 91:429-433.
35. Schneider E, Horton J, Yang CH, Nakagawa M, and Cowan KH (1994) Multidrug resistance-associated protein gene overexpression and reduced drug sensitivity of topoisomerase II in a human breast carcinoma MCF-7 cell line selected for etoposide resistance. Cancer Res 54:152-158.
36. Schurr E, Raymond M, Bell JC, and Gros P (1989) Characterization of the multidrug resistance protein expressed in cell clones stably transfected with the mouse mdr1 cDNA. Cancer Res 49:2729-2733.
37. Smitherman PK, Townsend AJ, Kute TE, and Morrow CS (2004) Role of multidrug resistance protein 2 (MRP2, ABCC2) in alkylating agent detoxification: MRP2 potentiates glutathione S-transferase A1-1-mediated resistance to chlorambucil cytotoxicity. J Pharmacol Exp Ther 308:260-267.
38. Yang CH, Schneider E, Kuo ML, Volk EL, Rocchi E, and Chen YC (2000) BCRP/MXR/ABCP expression in topotecan-resistant human breast carcinoma cells. Biochem Pharmacol 60:831-837.
39. Zaman GJR, Flens MJ, Van Leusden MR, De Haas M, Mulder HS, Lankelma J, Pinedo HM, Scheper RJ, Baas F, Broxterman HJ, et al. (1994) The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 91:8822-8826.
40. Zelcer N, Huisman MT, Reid G, Wielinga P, Breedveld P, Kuil A, Knipscheer P, Schellens JHM, Schinkel AH, and Borst P (2003) Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). J Biol Chem 278:23538-23544.
41. Zhou R, Wang Y, Gruber A, Larsson R, Castanos-Velez E, and Liliemark E (1999) Topoisomerase II-mediated alterations of K562 drug resistant sublines. Med Oncol 16:191-198.