Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance

International Journal of Cancer

Volumn 92, Issue 6, 2001, Pages 777-783

  Harbottle, Andrew ^a   Daly, Ann K ^a   Atherton, Kathryn ^a   Campbell, F Charles ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Acquired resistance; Doxorubicin; Glutathione S transferases; Transporters

Indexed keywords

CURCUMIN; DOXORUBICIN; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN; VERAPAMIL;

ARTICLE; CANCER CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME INHIBITION; ENZYME MECHANISM; GENE FUNCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CALCIUM CHANNEL BLOCKERS; COLORING AGENTS; CURCUMIN; CYTOSOL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; GENETIC VECTORS; GLUTATHIONE S-TRANSFERASE PI; GLUTATHIONE TRANSFERASE; HUMANS; IMMUNOBLOTTING; INHIBITORY CONCENTRATION 50; ISOENZYMES; LIVER; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; P-GLYCOPROTEIN; PHENOTYPE; PROTEIN TRANSPORT; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRAZOLIUM SALTS; THIAZOLES; TRANSFECTION; TUMOR CELLS, CULTURED; VERAPAMIL;

EID: 0035877114     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.1283     Document Type: Article

References (40)

1. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase-II. Science 1984;226:466-8.
2. Tritton TR, Yee G. The anticancer agent adriamycin can be actively cytotoxic without entering cells. Science 1982;217:248-50.
3. Awasthi S, Sharma R, Awasthi YC, Belli JA, Frenkel EP. The relationship of doxorubicin binding to membrane-lipids with drug-resistance. Cancer Letts 1992;63:109-16.
4. Fojo A, Akiyama S, Gottesman MM, Pastan I. Reduced drug accumulation in multiple drug-resistant human-KB carcinoma cell-lines. Cancer Res 1985;45:3002-7.
5. Cole SPC, Bhardwaj G, Gerlach JH, Mackie J, Grant CE, Almquist KC, et al. Overexpression of a transporter gene in a multidrug-resistant human lung-cancer cell-line. Science 1992;258:1650-4.
6. Hayes JD, Pulford DJ. The glutathione-S-transferase supergene family-regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug-resistance. Crit Rev Biochem Mol Biol 1995;30:445-600.
7. Black SM, Beggs JD, Hayes JD, Bartoszek A, Muramatsu M, Sakai M. et al. Expression of human glutathione S-transferases in Saccharomyces cerevisiae confers resistance to the anticancer drugs adriamycin and chlorambucil. Biochem J 1990;268:309-15.
8. Nakagawa K, Saijo N, Tsuchida S, Sakai M, Tsunokawa Y, Yokota J, et al. Glutathione-S-transferase pi as a determinant of drug resistance in transfectant cell lines. J Biol Chem 1990;265:4296-301.
9. O'Brien ML, Tew KD. Glutathione and related enzymes in multidrug resistance. Eur J Cancer 1996;32A:967-78.
10. Ruetz S, Brault M, Kast C, Hemenway C, Heitman J, Grant CE, et al. Functional expression of the multidrug resistance-associated protein in the yeast saccharomyces-cerevisiae. J Biol Chem 1996;271:4154-60.
11. Loe DW, Almquist KC, Deeley RG. Cole SPC. Multidrug-resistance protein (MRP)-mediated transport of leukotriene C-4 and chemotherapeutic-agents in membrane-vesicles - demonstration of glutathione-dependent vincristine transport. J Biol Chem 1996;271:9675-82.
12. Priebe W, Krawczyk M, Kuo MT, Yamane Y, Savaraj N, Ishikawa T. Doxorabicin- and daunorubicin-glutathione conjugates, but not unconjugated drugs, competitively inhibit leukotriene C-4 transport mediated by MRP/GS-X pump. Biochem Biophys Res Comm 1998;247: 859-63.
13. Bentley P, Thomas A, Thomas J. Failure to induce resistance to cytotoxic drugs in normal lymphocytes. Leukemia Res 1996; 20:645-8.
14. Abe Y, Ohnishi Y, Yoshimura M, Ota E, Ozeki Y, Oshika Y, et al. P-glycoprotein-mediated acquired multidrug resistance of human lung cancer cells in vivo. Br J Cancer 1996;74:1929-34.
15. Moscow JA, Townsend AJ, Cowan KH. Elevation of pi class glutathione S-transferase activity in human breast cancer cells by transfection of the GST pi gene and its effect on sensitivity to toxins. Mol Pharmacol 1989;36:22-8.
16. Fairchild CR, Moscow JA, O'Brien EE, Cowan KH. Multidrug resistance in cells transfected with human genes encoding a variant P-glycoprotein and glutathione S-transferase-pi. Mol Pharmacol 1990; 37:801-9.
17. Beaumont PO, Moore MJ, Ahmad K, Payne MM, Lee C, Riddick DS. Role of glutathione S-transferases in the resistance of human colon cancer cell lines to doxorubicin. Cancer Res 1998;58:947-55.
18. Doroshow JH, Metz MZ, Matsumoto L, Winters KA, Sakai M, Muramatsu M, et al. Transduction of NIH 3T3 cells with a retrovirus carrying both human Mdr1 and glutathione-S-transferase-pi produces broad-range multidrug-resistance. Cancer Res 1995;55:4073-8.
19. Niitsu Y, Takahashi Y, Ban N, Takayama T, Saito T, Katahira T, et al. A proof of glutathione S-transferase-pi-related multidrug resistance by transfer of antisense gene to cancer cells and sense gene to bone marrow stem cell. Chem Biol Interact 1998;111-2, 325-32.
20. Redmond A, Moran E, Clynes M, Multiple-drug resistance in the human ovarian-carcinoma cell-line Oaw42-a. Eur J Cancer 1993;29A: 1078-81.
21. Sieuwerts AM, Klijn JGM, Peters HA, Foekens JA. The Mtt tetrazolium salt assay scrutinized - how to use this assay reliably to measure metabolic-activity of cell-cultures in-vitro for the assessment of growth-characteristics, lc50-values and cell-survival. Eur J Clin Chem Clin Biochem 1995;33:813-23.
22. Lee JS, Paull K, Alvarez M, Hose C, Monks A, Grever M, et al. Rhodamine efflux patterns predict P-glycoprotein substrates in the National Cancer Institute drug screen. Mol Pharmacol 1994;46:627-38.
23. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249: 7130-9.
24. Germann UA, Gottesman MM, Pastan I. Expression of a multidrug resistance-adenosine deaminase fusion gene. J Biol Chem 1989;264: 7418-24.
25. Van Iersel M, Ploemen J, Struik I, Van Amersfoort C, Keyzer AE, Schefferlie JG, et al. Inhibition of glutathione S-transferase activity in human melanoma cells by alpha,beta-unsaturated carbonyl derivatives. Effects of acrolein, cinnamaldehyde, citral, crotonaldehyde, curcumin, ethacrynic acid, and trans-2-hexenal. Chem Biol Interact 1996;102:117-32.
26. Awasthi S, Pandya U, Singhal SS, Lin JT, Thiviyanathan V, Seifert WE, et al. Curcumin-glutathione interactions and the role of human glutathione S-transferase P1-1. Chem Biol Interact 2000;128:19-38.
27. Muller M, Meijer C, Zaman GJ, Borst P, Scheper RJ, Mulder NH, et al. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 1994;91:13033-7.
28. Muller I, Jenner A, Bruchelt G, Niethammer D, Halliwell B. Effect of concentration on the cytotoxic mechanism of doxorubicin-apoptosis and oxidative DNA damage. Biochem Biophys Res Comm 1997;230: 254-7.
29. Hao XY, Bergh J, Brodin O, Hellman U, Mannervik B. Acquired-resistance to cisplatin and doxorubicin in a small-cell lung-cancer cell-line is correlated to elevated expression of glutathione-linked detoxification enzymes. Carcinogenesis 1994;15:1167-73.
30. Wang K. Ramji S, Bhathena A, Lee C, Riddick DS. Glutathione S-transferases in wild-type and doxorubicin-resistant MCF-7 human breast cancer cell lines. Xenobiotica 1999;29:155-70.
31. Gaudiano G, Resing K, Koch TH. Reaction of anthracycline antitumor drugs with reduced glutathione-formation of aglycon conjugates. J Amer Chem Soc 1994;116:6537-44.
32. Ogretmen B, Bahadori HR, McCauley MD, Boylan A, Green MR, Safa AR. Co-ordinated over-expression of the MRP and gamma-glutamylcysteine synthetase genes, but not MDR1, correlates with doxorubicin resistance in human malignant mesothelioma cell lines. Im J Cancer 1998;75:757-61.
33. O'Brien M, Kruh GD, Tew KD. The influence of coordinate overex-pression of glutathione phase II detoxification gene products on drug resistance. J Pharmacol Exp Therap 2000;294:480-7.
34. Townsend AJ, Tu CPD, Cowan KH. Expression of human mu or alpha class glutathione S-transferases in stably transfected human Mcf-7 breast-cancer cells - effect on cellular-sensitivity to cytotoxic agents. Mol Pharmacol 1992;41:230-6.
35. Raghu G, Pierre-Jerome M, Dordal MS, Simonian P, Bauer KD, Winter JN. P-glycoprotein and alterations in the glutathione/glutathione-peroxidase cycle underlie doxorubicin resistance in HL-60-R, a subclone of the HL-60 human leukemia cell line. Int J Cancer 1993; 53:804-11.
36. Sato H, Preisler H, Day R, Raza A, Larson R, Browman G, et al. MDR1 transcript levels as an indication of resistant disease in acute myelogenous leukaemia. Br J Haematol 1990;75:340-5.
37. Cheng XS, Kigawa J, Minagawa Y, Kanamori Y, Itamochi H, Okada M, et al. Glutathione S-transferase-pi expression and glutathione concentration in ovarian carcinoma before and after chemotherapy. Cancer 1997;79:521-7.
38. Ling V. Multidrug resistance: molecular mechanisms and clinical relevance. Cancer Chemother Pharmacol 1997;40:S3-S8.
39. Sonneveld P, Durie BG, Lokhorst HM, Marie JP, Solbu G, Suciu S, et al. Modulation of multidrug-resistant multiple myeloma by cyclosporin. The Leukaemia Group of the EORTC and the HOVON [see comments]. Lancet 1992;340:255-9.
40. Gupta V, Jani JP, Jacobs S, Levitt M, Fields L, Awasthi S, et al. Activity of melphalan in combination with the glutathione s-transferase inhibitor, sulphasalazine. Cancer Chemother Pharmacol 1995; 36:13-9.