Combined action and regulation of phase II enzymes and multidrug resistance proteins in multidrug resistance in cancer

Cancer Treatment Reviews

Volumn 34, Issue 6, 2008, Pages 505-520

  Meijerman, Irma ^a   Beijnen, Jos H ^a,b   Schellens, Jan H M ^a,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b SLOTERVAART HOSPITAL   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Multidrug resistance; Multidrug resistance proteins; Nrf2; Oncolytic drugs; Phase II enzymes

Indexed keywords

ABC TRANSPORTER; ANTHRACYCLINE DERIVATIVE; ANTINEOPLASTIC AGENT; ARSENIC TRIOXIDE; BREAST CANCER RESISTANCE PROTEIN; BUTHIONINE SULFOXIMINE; CAMPTOTHECIN DERIVATIVE; CISPLATIN; CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME P450; CYTOCHROME P450 3A4; DAUNORUBICIN; DOXORUBICIN; EPIPODOPHYLLOTOXIN DERIVATIVE; ETOPOSIDE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; TAMOXIFEN; TENIPOSIDE; TRANSCRIPTION FACTOR NRF2; UNINDEXED DRUG; VINCRISTINE;

ANTIOXIDANT RESPONSIVE ELEMENT; CANCER CELL; CANCER PATIENT; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MULTIDRUG RESISTANCE; NONHUMAN; PATIENT CARE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HUMANS; NEOPLASMS; P-GLYCOPROTEINS;

EID: 50849127129     PISSN: 03057372     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ctrv.2008.03.002     Document Type: Review

References (179)

1. de Grouw E.P., Raaijmakers M.H., Boezeman J.B., van der Reijden B.A., van de Locht L.T., de Witte T.J., et al. Preferential expression of a high number of ATP binding cassette transporters in both normal and leukemic CD34+CD38-cells. Leukemia 20 (2006) 750-754
2. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., and Gottesman M.M. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5 (2006) 219-234
3. Tew K.D. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res 54 (1994) 4313-4320
4. Tokizane T., Shiina H., Igawa M., Enokida H., Urakami S., Kawakami T., et al. Cytochrome P450 1B1 is overexpressed and regulated by hypomethylation in prostate cancer. Clin Cancer Res 11 (2005) 5793-5801
5. Gibson P., Gill J.H., Khan P.A., Seargent J.M., Martin S.W., Batman P.A., et al. Cytochrome P450 1B1 (CYP1B1) is overexpressed in human colon adenocarcinomas relative to normal colon: implications for drug development. Mol Cancer Ther 2 (2003) 527-534
6. Murray G.I., Taylor M.C., McFadyen M.C., McKay J.A., Greenlee W.F., Burke M.D., et al. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res 57 (1997) 3026-3031
7. Drummond J.T. Genomic amplification of the human DHFR/MSH3 locus remodels mismatch recognition and repair activities. Adv Enzyme Regul 39 (1999) 129-141
8. Pandit B., Roy M., Dutta J., Padhi B.K., Bhoumik G., and Bhattacharyya N.P. Co-amplification of dhfr and a homologue of hmsh3 in a Chinese hamster methotrexate-resistant cell line correlates with resistance to a range of chemotherapeutic drugs. Cancer Chemother Pharmacol 48 (2001) 312-318
9. Wosikowski K., Schuurhuis D., Kops G.J., Saceda M., and Bates S.E. Altered gene expression in drug-resistant human breast cancer cells. Clin Cancer Res 3 (1997) 2405-2414
10. Pommier Y., Leteurtre F., Fesen M.R., Fujimori A., Bertrand R., Solary E., et al. Cellular determinants of sensitivity and resistance to DNA topoisomerase inhibitors. Cancer Invest 12 (1994) 530-542
11. Rosell R., Taron M., Ariza A., Barnadas A., Mate J.L., Reguart N., et al. Molecular predictors of response to chemotherapy in lung cancer. Semin Oncol 31 (2004) 20-27
12. Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J Biol Chem 269 (1994) 787-790
13. Li Q., Tsang B., Bostick-Bruton F., and Reed E. Modulation of excision repair cross complementation group 1 (ERCC-1) mRNA expression by pharmacological agents in human ovarian carcinoma cells. Biochem Pharmacol 57 (1999) 347-353
14. O'Connor P.M., Jackman J., Bae I., Myers T.G., Fan S., Mutoh M., et al. Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res 57 (1997) 4285-4300
15. Ding Z., Yang X., Pater A., and Tang S.C. Resistance to apoptosis is correlated with the reduced caspase-3 activation and enhanced expression of antiapoptotic proteins in human cervical multidrug-resistant cells. Biochem Biophys Res Commun 270 (2000) 415-420
16. Warmann S.W., Frank H., Heitmann H., Ruck P., Herberts T., Seitz G., et al. Bcl-2 gene silencing in pediatric epithelial liver tumors. J Surg Res 144 (2008) 43-48
17. Davis J.M., Navolanic P.M., Weinstein-Oppenheimer C.R., Steelman L.S., Hu W., Konopleva M., et al. Raf-1 and Bcl-2 induce distinct and common pathways that contribute to breast cancer drug resistance. Clin Cancer Res 9 (2003) 1161-1170
18. Gottesman M.M., Fojo T., and Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2 (2002) 48-58
19. Luqmani Y.A. Mechanisms of drug resistance in cancer chemotherapy. Med Princ Pract 14 Suppl. 1 (2005) 35-48
20. Riddick D.S., Lee C., Ramji S., Chinje E.C., Cowen R.L., Williams K.J., et al. Cancer chemotherapy and drug metabolism. Drug Metab Dispos 33 (2005) 1083-1096
21. Stavrovskaya A.A. Cellular mechanisms of multidrug resistance of tumor cells. Biochemistry (Mosc) 65 (2000) 95-106
22. Schuetz E.G., Beck W.T., and Schuetz J.D. Modulators and substrates of P-glycoprotein and cytochrome P4503A coordinately up-regulate these proteins in human colon carcinoma cells. Mol Pharmacol 49 (1996) 311-318
23. Benet L.Z., Cummins C.L., and Wu C.Y. Unmasking the dynamic interplay between efflux transporters and metabolic enzymes. Int J Pharm 277 (2004) 3-9
24. Cerveny L., Svecova L., Anzenbacherova E., Vrzal R., Staud F., Dvorak Z., et al. Valproic acid induces CYP3A4 and MDR1 gene expression by activation of constitutive androstane receptor and pregnane X receptor pathways. Drug Metab Dispos 35 (2007) 1032-1041
25. Synold T.W., Dussault I., and Forman B.M. The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nat Med 7 (2001) 584-590
26. Harmsen S., Meijerman I., Beijnen J.H., and Schellens J.H. The role of nuclear receptors in pharmacokinetic drug-drug interactions in oncology. Cancer Treat Rev 33 (2007) 369-380
27. Larsen L.A., Christiansen M., Vuust J., and Andersen P.S. Recent developments in high-throughput mutation screening. Pharmacogenomics 2 (2001) 387-399
28. Nagaoka R., Iwasaki T., Rokutanda N., Takeshita A., Koibuchi Y., Horiguchi J., et al. Tamoxifen activates CYP3A4 and MDR1 genes through steroid and xenobiotic receptor in breast cancer cells. Endocrine 30 (2006) 261-268
29. Mensah-Osman E.J., Thomas D.G., Tabb M.M., Larios J.M., Hughes D.P., Giordano T.J., et al. Expression levels and activation of a PXR variant are directly related to drug resistance in osteosarcoma cell lines. Cancer 109 (2007) 957-965
30. Rappa G., Lorico A., Flavell R.A., and Sartorelli A.C. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 57 (1997) 5232-5237
31. Morrow C.S., Peklak-Scott C., Bishwokarma B., Kute T.E., Smitherman P.K., and Townsend A.J. Multidrug resistance protein 1 (MRP1, ABCC1) mediates resistance to mitoxantrone via glutathione-dependent drug efflux. Mol Pharmacol 69 (2006) 1499-1505
32. NCBI The Human ATP-binding Casette (ABC) Transporter Superfamily - ABCC genes. ; 2008.
33. Yabuuchi H., Takayanagi S., Yoshinaga K., Taniguchi N., Aburatani H., and Ishikawa T. ABCC13, an unusual truncated ABC transporter, is highly expressed in fetal human liver. Biochem Biophys Res Commun 299 (2002) 410-417
34. Annilo T., and Dean M. Degeneration of an ATP-binding cassette transporter gene, ABCC13, in different mammalian lineages. Genomics 84 (2004) 34-46
35. Chan J.Y., Chu A.C., and Fung K.P. Inhibition of P-glycoprotein expression and reversal of drug resistance of human hepatoma HepG2 cells by multidrug resistance gene (mdr1) antisense RNA. Life Sci 67 (2000) 2117-2124
36. Deeley R.G., Westlake C., and Cole S.P. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86 (2006) 849-899
37. Schinkel A.H., and Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55 (2003) 3-29
38. Borst P., and Elferink R.O. Mammalian ABC transporters in health and disease. Annu Rev Biochem 71 (2002) 537-592
39. Devling T.W., Lindsay C.D., McLellan L.I., McMahon M., and Hayes J.D. Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proc Natl Acad Sci USA 102 (2005) 7280-5A
40. Zaman G.J., Lankelma J., van Tellingen O., Beijnen J., Dekker H., Paulusma C., et al. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc Natl Acad Sci USA 92 (1995) 7690-7694
41. Zeng H., Bain L.J., Belinsky M.G., and Kruh G.D. Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents. Cancer Res 59 (1999) 5964-5967
42. Townsend D.M., Tew K.D., and Tapiero H. The importance of glutathione in human disease. Biomed Pharmacother 57 (2003) 145-155
43. McIlwain C.C., Townsend D.M., and Tew K.D. Glutathione S-transferase polymorphisms: cancer incidence and therapy. Oncogene 25 (2006) 1639-1648
44. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu Rev Pharmacol Toxicol 45 (2005) 51-88
45. Pool-Zobel B., Veeriah S., and Bohmer F.D. Modulation of xenobiotic metabolising enzymes by anticarcinogens - focus on glutathione S-transferases and their role as targets of dietary chemoprevention in colorectal carcinogenesis. Mutat Res 591 (2005) 74-92
46. Manoharan T.H., Welch P.J., Gulick A.M., Puchalski R.B., Lathrop A.L., and Fahl W.E. Expression of tandem glutathione S-transferase recombinant genes in COS cells for analysis of efficiency of protein expression and associated drug resistance. Mol Pharmacol 39 (1991) 461-467
47. Ban N., Takahashi Y., Takayama T., Kura T., Katahira T., Sakamaki S., et al. Transfection of glutathione S-transferase (GST)-pi antisense complementary DNA increases the sensitivity of a colon cancer cell line to adriamycin, cisplatin, melphalan, and etoposide. Cancer Res 56 (1996) 3577-3582
48. Kisara S., Furusawa S., Murata R., Ogata M., Hikichi N., Takayanagi Y., et al. Combined effects of buthionine sulfoximine and cepharanthine on cytotoxic activity of doxorubicin to multidrug-resistant cells. Oncol Res 7 (1995) 191-200
49. Hassan S., Dhar S., Sandstrom M., Arsenau D., Budnikova M., Lokot I., et al. Cytotoxic activity of a new paclitaxel formulation, Pacliex, in vitro and in vivo. Cancer Chemother Pharmacol 55 (2005) 47-54
50. Vanhoefer U., Cao S., Minderman H., Toth K., Skenderis II B.S., et al. d, l-buthionine-(S, R)-sulfoximine potentiates in vivo the therapeutic efficacy of doxorubicin against multidrug resistance protein-expressing tumors. Clin Cancer Res 2 (1996) 1961-1968
51. Chuman Y., Chen Z.S., Seto K., Sumizawa T., Furukawa T., Tani A., et al. Reversal of MRP-mediated vincristine resistance in KB cells by buthionine sulfoximine in combination with PAK-104P. Cancer Lett 129 (1998) 69-76
52. Akan I., Akan S., Akca H., Savas B., and Ozben T. Multidrug resistance-associated protein 1 (MRP1) mediated vincristine resistance: effects of N-acetylcysteine and buthionine sulfoximine. Cancer Cell Int 5 (2005) 22
53. Voehringer D.W., Hirschberg D.L., Xiao J., Lu Q., Roederer M., Lock C.B., et al. Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci USA 97 (2000) 2680-2685
54. Kodym R., Calkins P., and Story M. The cloning and characterization of a new stress response protein. A mammalian member of a family of theta class glutathione S-transferase-like proteins. J Biol Chem 274 (1999) 5131-5137
55. Cumming R.C., Lightfoot J., Beard K., Youssoufian H., O'Brien P.J., and Buchwald M. Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1. Nat Med 7 (2001) 814-820
56. Potapova O., Haghighi A., Bost F., Liu C., Birrer M.J., Gjerset R., et al. The Jun kinase/stress-activated protein kinase pathway functions to regulate DNA repair and inhibition of the pathway sensitizes tumor cells to cisplatin. J Biol Chem 272 (1997) 14041-14044
57. Cummings J., Boyd G., Ethell B.T., Macpherson J.S., Burchell B., Smyth J.F., et al. Enhanced clearance of topoisomerase I inhibitors from human colon cancer cells by glucuronidation. Biochem Pharmacol 63 (2002) 607-613
58. Cummings J., Ethell B.T., Jardine L., Boyd G., Macpherson J.S., Burchell B., et al. Glucuronidation as a mechanism of intrinsic drug resistance in human colon cancer: reversal of resistance by food additives. Cancer Res 63 (2003) 8443-8450
59. Jedlitschky G., Leier I., Buchholz U., Center M., and Keppler D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res 54 (1994) 4833-4836
60. Barnouin K., Leier I., Jedlitschky G., Pourtier-Manzanedo A., Konig J., Lehmann W.D., et al. Multidrug resistance protein-mediated transport of chlorambucil and melphalan conjugated to glutathione. Br J Cancer 77 (1998) 201-209
61. Muller M., Meijer C., Zaman G.J., Borst P., Scheper R.J., Mulder N.H., 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 91 (1994) 13033-13037
62. Keppler D., Leier I., and Jedlitschky G. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol Chem 378 (1997) 787-791
63. Hayes J.D., and Pulford D.J. 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 30 (1995) 445-600
64. Tew K.D., Monks A., Barone L., Rosser D., Akerman G., Montali J.A., et al. Glutathione-associated enzymes in the human cell lines of the National Cancer Institute Drug Screening Program. Mol Pharmacol 50 (1996) 149-159
65. Kuo M.T., Bao J., Furuichi M., Yamane Y., Gomi A., Savaraj N., et al. Frequent coexpression of MRP/GS-X pump and gamma-glutamylcysteine synthetase mRNA in drug-resistant cells, untreated tumor cells, and normal mouse tissues. Biochem Pharmacol 55 (1998) 605-615
66. Ishikawa T., Bao J.J., Yamane Y., Akimaru K., Frindrich K., Wright C.D., et al. Coordinated induction of MRP/GS-X pump and gamma-glutamylcysteine synthetase by heavy metals in human leukemia cells. J Biol Chem 271 (1996) 14981-14988
67. Leyland-Jones B.R., Townsend A.J., Tu C.P., Cowan K.H., and Goldsmith M.E. Antineoplastic drug sensitivity of human MCF-7 breast cancer cells stably transfected with a human alpha class glutathione S-transferase gene. Cancer Res 51 (1991) 587-594
68. Moscow J.A., Townsend A.J., and Cowan K.H. 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 36 (1989) 22-28
69. Townsend A.J., Tu C.P., and Cowan K.H. 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 41 (1992) 230-236
70. Morrow C.S., Smitherman P.K., Diah S.K., Schneider E., and Townsend A.J. 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 273 (1998) 20114-20120
71. Dekant W. Chemical-induced nephrotoxicity mediated by glutathione S-conjugate formation. Toxicol Lett 124 (2001) 21-36
72. Monks T.J., Anders M.W., Dekant W., Stevens J.L., Lau S.S., and van Bladeren P.J. Glutathione conjugate mediated toxicities. Toxicol Appl Pharmacol 106 (1990) 1-19
73. Priebe W., Krawczyk M., Kuo M.T., Yamane Y., Savaraj N., and Ishikawa T. Doxorubicin- and daunorubicin-glutathione conjugates, but not unconjugated drugs, competitively inhibit leukotriene C4 transport mediated by MRP/GS-X pump. Biochem Biophys Res Commun 247 (1998) 859-863
74. Smitherman P.K., Townsend A.J., Kute T.E., and Morrow C.S. 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 (2004) 260-267
75. Morrow C.S., Diah S., Smitherman P.K., Schneider E., and Townsend A.J. Multidrug resistance protein and glutathione S-transferase P1-1 act in synergy to confer protection from 4-nitroquinoline 1-oxide toxicity. Carcinogenesis 19 (1998) 109-115
76. Morrow C.S., Smitherman P.K., and Townsend A.J. Role of multidrug-resistance protein 2 in glutathione S-transferase P1-1-mediated resistance to 4-nitroquinoline 1-oxide toxicities in HepG2 cells. Mol Carcinog 29 (2000) 170-178
77. Peklak-Scott C., Townsend A.J., and Morrow C.S. 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 (2005) 4426-4433
78. Morrow C.S., Smitherman P.K., and Townsend A.J. 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 56 (1998) 1013-1021
79. O'Brien M., Kruh G.D., and Tew K.D. The influence of coordinate overexpression of glutathione phase II detoxification gene products on drug resistance. J Pharmacol Exp Ther 294 (2000) 480-487
80. Harbottle A., Daly A.K., Atherton K., and Campbell F.C. Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int J Cancer 92 (2001) 777-783
81. Liu J., Chen H., Miller D.S., Saavedra J.E., Keefer L.K., Johnson D.R., et al. Overexpression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol Pharmacol 60 (2001) 302-309
82. Depeille P., Cuq P., Mary S., Passagne I., Evrard A., Cupissol D., et al. Glutathione S-transferase M1 and multidrug resistance protein 1 act in synergy to protect melanoma cells from vincristine effects. Mol Pharmacol 65 (2004) 897-905
83. Paumi C.M., Ledford B.G., Smitherman P.K., Townsend A.J., and Morrow C.S. 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 (2001) 7952-7956
84. Rappa G., Gamcsik M.P., Mitina R.L., Baum C., Fodstad O., and Lorico A. Retroviral transfer of MRP1 and gamma-glutamyl cysteine synthetase modulates cell sensitivity to l-buthionine-S, R-sulphoximine (BSO): new rationale for the use of BSO in cancer therapy. Eur J Cancer 39 (2003) 120-128
85. Benderra Z., Trussardi A., Morjani H., Villa A.M., Doglia S.M., and Manfait M. Regulation of cellular glutathione modulates nuclear accumulation of daunorubicin in human MCF7 cells overexpressing multidrug resistance associated protein. Eur J Cancer 36 (2000) 428-434
86. Akan I., Akan S., Akca H., Savas B., and Ozben T. N-Acetylcysteine enhances multidrug resistance-associated protein 1 mediated doxorubicin resistance. Eur J Clin Invest 34 (2004) 683-689
87. Konig J., Nies A.T., Cui Y., Leier I., and Keppler D. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1461 (1999) 377-394
88. Chu X.Y., Kato Y., Niinuma K., Sudo K.I., Hakusui H., and Sugiyama Y. Multispecific organic anion transporter is responsible for the biliary excretion of the camptothecin derivative irinotecan and its metabolites in rats. J Pharmacol Exp Ther 281 (1997) 304-314
89. Chu X.Y., Kato Y., and Sugiyama Y. Multiplicity of biliary excretion mechanisms for irinotecan, CPT-11, and its metabolites in rats. Cancer Res 57 (1997) 1934-1938
90. Sharom F.J., Yu X., Lu P., Liu R., Chu J.W., Szabo K., et al. Interaction of the P-glycoprotein multidrug transporter (MDR1) with high affinity peptide chemosensitizers in isolated membranes, reconstituted systems, and intact cells. Biochem Pharmacol 58 (1999) 571-586
91. van de Wetering K., Zelcer N., Kuil A., Feddema W., Hillebrand M., Vlaming M.L., et al. Multidrug resistance proteins 2 and 3 provide alternative routes for hepatic excretion of morphine-glucuronides. Mol Pharmacol 72 (2007) 387-394
92. Zelcer N., van de Wetering K., Hillebrand M., Sarton E., Kuil A., Wielinga P.R., et al. Mice lacking multidrug resistance protein 3 show altered morphine pharmacokinetics and morphine-6-glucuronide antinociception. Proc Natl Acad Sci USA 102 (2005) 7274-7279
93. Cummings J., Zelcer N., Allen J.D., Yao D., Boyd G., Maliepaard M., et al. Glucuronidation as a mechanism of intrinsic drug resistance in colon cancer cells: contribution of drug transport proteins. Biochem Pharmacol 67 (2004) 31-39
94. Theodoulou F.L., Clark I.M., He X.L., Pallett K.E., Cole D.J., and Hallahan D.L. Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manag Sci 59 (2003) 202-214
95. Wang S., Hartley D.P., Ciccotto S.L., Vincent S.H., Franklin R.B., and Kim M.S. Induction of hepatic phase II drug-metabolizing enzymes by 1,7-phenanthroline in rats is accompanied by induction of MRP3. Drug Metab Dispos 31 (2003) 773-775
96. Rushmore T.H., Morton M.R., and Pickett C.B. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 266 (1991) 11632-11639
97. Rushmore T.H., King R.G., Paulson K.E., and Pickett C.B. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc Natl Acad Sci USA 87 (1990) 3826-3830
98. Wasserman W.W., and Fahl W.E. Functional antioxidant responsive elements. Proc Natl Acad Sci USA 94 (1997) 5361-5366
99. Kwak M.K., Wakabayashi N., Itoh K., Motohashi H., Yamamoto M., and Kensler T.W. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J Biol Chem 278 (2003) 8135-8145
100. Moinova H.R., and Mulcahy R.T. An electrophile responsive element (EpRE) regulates beta-naphthoflavone induction of the human gamma-glutamylcysteine synthetase regulatory subunit gene. Constitutive expression is mediated by an adjacent AP-1 site. J Biol Chem 273 (1998) 14683-14689
101. Yueh M.F., and Tukey R.H. Nrf2-Keap1 signaling pathway regulates human UGT1A1 expression in vitro and in transgenic UGT1 mice. J Biol Chem 282 (2007) 8749-8758
102. Vollrath V., Wielandt A.M., Iruretagoyena M., and Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 395 (2006) 599-609
103. Maher J.M., Dieter M.Z., Aleksunes L.M., Slitt A.L., Guo G., Tanaka Y., et al. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 46 (2007) 1597-1610
104. Hayashi A., Suzuki H., Itoh K., Yamamoto M., and Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun 310 (2003) 824-829
105. Kauffmann H.M., Pfannschmidt S., Zoller H., Benz A., Vorderstemann B., Webster J.I., et al. Influence of redox-active compounds and PXR-activators on human MRP1 and MRP2 gene expression. Toxicology 171 (2002) 137-146
106. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236 (1997) 313-322
107. Hayes J.D., and McMahon M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett 174 (2001) 103-113
108. Chanas S.A., Jiang Q., McMahon M., McWalter G.K., McLellan L.I., Elcombe C.R., et al. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem J 365 (2002) 405-416
109. Chan K., Han X.D., and Kan Y.W. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 98 (2001) 4611-4616
110. Hayes J.D., Chanas S.A., Henderson C.J., McMahon M., Sun C., Moffat G.J., et al. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem Soc Trans 28 (2000) 33-41
111. McMahon M., Itoh K., Yamamoto M., Chanas S.A., Henderson C.J., McLellan L.I., et al. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 61 (2001) 3299-3307
112. Ramos-Gomez M., Kwak M.K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., et al. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98 (2001) 3410-3415
113. Cho H.Y., Jedlicka A.E., Reddy S.P., Kensler T.W., Yamamoto M., Zhang L.Y., et al. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26 (2002) 175-182
114. Moinova H.R., and Mulcahy R.T. Up-regulation of the human gamma-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element. Biochem Biophys Res Commun 261 (1999) 661-668
115. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 59 (2001) 169-177
116. Chan J.Y., and Kwong M. Impaired expression of glutathione synthetic enzyme genes in mice with targeted deletion of the Nrf2 basic-leucine zipper protein. Biochim Biophys Acta 1517 (2000) 19-26
117. McWalter G.K., Higgins L.G., McLellan L.I., Henderson C.J., Song L., Thornalley P.J., et al. Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J Nutr 134 (2004) 3499S-3506S
118. Thimmulappa R.K., Mai K.H., Srisuma S., Kensler T.W., Yamamoto M., and Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62 (2002) 5196-5203
119. Fisher C.D., Augustine L.M., Maher J.M., Nelson D.M., Slitt A.L., Klaassen C.D., et al. Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab Dispos 35 (2007) 995-1000
120. Chen C., Yu R., Owuor E.D., and Kong A.N. Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharm Res 23 (2000) 605-612
121. Chen C., and Kong A.N. Dietary chemopreventive compounds and ARE/EpRE signaling. Free Radic Biol Med 36 (2004) 1505-1516
122. Nishinaka T., Ichijo Y., Ito M., Kimura M., Katsuyama M., Iwata K., et al. Curcumin activates human glutathione S-transferase P1 expression through antioxidant response element. Toxicol Lett 170 (2007) 238-247
123. Buetler T.M., Gallagher E.P., Wang C., Stahl D.L., Hayes J.D., and Eaton D.L. Induction of phase I and phase II drug-metabolizing enzyme mRNA, protein, and activity by BHA, ethoxyquin, and oltipraz. Toxicol Appl Pharmacol 135 (1995) 45-57
124. Wielandt A.M., Vollrath V., Farias M., and Chianale J. Bucillamine induces glutathione biosynthesis via activation of the transcription factor Nrf2. Biochem Pharmacol 72 (2006) 455-462
125. Bock K.W., Eckle T., Ouzzine M., and Fournel-Gigleux S. Coordinate induction by antioxidants of UDP-glucuronosyltransferase UGT1A6 and the apical conjugate export pump MRP2 (multidrug resistance protein 2) in Caco-2 cells. Biochem Pharmacol 59 (2000) 467-470
126. Tirona R.G., and Kim R.B. Nuclear receptors and drug disposition gene regulation. J Pharm Sci 94 (2005) 1169-1186
127. Klaassen C.D., and Slitt A.L. Regulation of hepatic transporters by xenobiotic receptors. Curr Drug Metab 6 (2005) 309-328
128. Zhou J., Zhang J., and Xie W. Xenobiotic nuclear receptor-mediated regulation of UDP-glucuronosyl-transferases. Curr Drug Metab 6 (2005) 289-298
129. Shibayama Y., Ikeda R., Motoya T., and Yamada K. St. John's Wort (Hypericum perforatum) induces overexpression of multidrug resistance protein 2 (MRP2) in rats: a 30-day ingestion study. Food Chem Toxicol 42 (2004) 995-1002
130. Kohle C., and Bock K.W. Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem Pharmacol 73 (2007) 1853-1862
131. McLellan L.I., and Wolf C.R. Glutathione and glutathione-dependent enzymes in cancer drug resistance. Drug Resist Updat 2 (1999) 153-164
132. Sparreboom A., Cox M.C., Acharya M.R., and Figg W.D. Herbal remedies in the United States: potential adverse interactions with anticancer agents. J Clin Oncol 22 (2004) 2489-2503
133. Wang X.J., Hayes J.D., and Wolf C.R. Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents. Cancer Res 66 (2006) 10983-10994
134. Zhang K., Mack P., and Wong K.P. Glutathione-related mechanisms in cellular resistance to anticancer drugs. Int J Oncol 12 (1998) 871-882
135. Kwak M.K., Wakabayashi N., and Kensler T.W. Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutat Res 555 (2004) 133-148
136. Kretschmer X.C., and Baldwin W.S. CAR and PXR: xenosensors of endocrine disrupters?. Chem Biol Interact 155 (2005) 111-128
137. McMillan B.J., and Bradfield C.A. The aryl hydrocarbon receptor sans xenobiotics: endogenous function in genetic model systems. Mol Pharmacol 72 (2007) 487-498
138. Allen J.D., Brinkhuis R.F., van Deemter L., Wijnholds J., and Schinkel A.H. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res 60 (2000) 5761-5766
139. Lorico A., Rappa G., Flavell R.A., and Sartorelli A.C. Double knockout of the MRP gene leads to increased drug sensitivity in vitro. Cancer Res 56 (1996) 5351-5355
140. Hooijberg J.H., Broxterman H.J., Kool M., Assaraf Y.G., Peters G.J., Noordhuis P., et al. Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 59 (1999) 2532-2535
141. van Tellingen O., Buckle T., Jonker J.W., van der Valk M.A., and Beijnen J.H. P-glycoprotein and Mrp1 collectively protect the bone marrow from vincristine-induced toxicity in vivo. Br J Cancer 89 (2003) 1776-1782
142. Wijnholds J., Evers R., van Leusden M.R., Mol C.A., Zaman G.J., Mayer U., et al. Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3 (1997) 1275-1279
143. Liedert B., Materna V., Schadendorf D., Thomale J., and Lage H. Overexpression of cMOAT (MRP2/ABCC2) is associated with decreased formation of platinum-DNA adducts and decreased G2-arrest in melanoma cells resistant to cisplatin. J Invest Dermatol 121 (2003) 172-176
144. Huisman M.T., Chhatta A.A., van Tellingen O., Beijnen J.H., and Schinkel A.H. MRP2 (ABCC2) transports taxanes and confers paclitaxel resistance and both processes are stimulated by probenecid. Int J Cancer 116 (2005) 824-829
145. Choi H.K., Yang J.W., Roh S.H., Han C.Y., and Kang K.W. Induction of multidrug resistance associated protein 2 in tamoxifen-resistant breast cancer cells. Endocr Relat Cancer 14 (2007) 293-303
146. Kawabe T., Chen Z.S., Wada M., Uchiumi T., Ono M., Akiyama S., et al. Enhanced transport of anticancer agents and leukotriene C4 by the human canalicular multispecific organic anion transporter (cMOAT/MRP2). FEBS Lett 456 (1999) 327-331
147. Kool M., de Haas M., Scheffer G.L., Scheper R.J., van Eijk M.J., Juijn J.A., et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res 57 (1997) 3537-3547
148. Koike K., Kawabe T., Tanaka T., Toh S., Uchiumi T., Wada M., et al. A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res 57 (1997) 5475-5479
149. Townsend D.M., and Tew K.D. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22 (2003) 7369-7375
150. Dulik D.M., Fenselau C., and Hilton J. Characterization of melphalan-glutathione adducts whose formation is catalyzed by glutathione transferases. Biochem Pharmacol 35 (1986) 3405-3409
151. Bolton A.E., Peng B., Hubert M., Krebs-Brown A., Capdeville R., Keller U., et al. Effect of rifampicin on the pharmacokinetics of imatinib mesylate (Gleevec, STI571) in healthy subjects. Cancer Chemother Pharmacol 53 (2004) 102-106
152. Zhang K., and Wong K.P. Glutathione conjugation of chlorambucil: measurement and modulation by plant polyphenols. Biochem J 325 Pt 2 (1997) 417-422
153. Zhang K., Yang E.B., Wong K.P., and Mack P. GSH, GSH-related enzymes and GS-X pump in relation to sensitivity of human tumor cell lines to chlorambucil and adriamycin. Int J Oncol 14 (1999) 861-867
154. Schisselbauer J.C., Silber R., Papadopoulos E., Abrams K., LaCreta F.P., and Tew K.D. Characterization of glutathione S-transferase expression in lymphocytes from chronic lymphocytic leukemia patients. Cancer Res 50 (1990) 3562-3568
155. Horton J.K., Roy G., Piper J.T., Van Houten B., Awasthi Y.C., Mitra S., et al. Characterization of a chlorambucil-resistant human ovarian carcinoma cell line overexpressing glutathione S-transferase mu. Biochem Pharmacol 58 (1999) 693-702
156. Gamcsik M.P., Hamill T.G., and Colvin M. NMR studies of the conjugation of mechlorethamine with glutathione. J Med Chem 33 (1990) 1009-1014
157. Dirven H.A., van Ommen B., and van Bladeren P.J. Involvement of human glutathione S-transferase isoenzymes in the conjugation of cyclophosphamide metabolites with glutathione. Cancer Res 54 (1994) 6215-6220
158. Dirven H.A., Venekamp J.C., van Ommen B., and van Bladeren P.J. The interaction of glutathione with 4-hydroxycyclophosphamide and phosphoramide mustard, studied by 31P nuclear magnetic resonance spectroscopy. Chem Biol Interact 93 (1994) 185-196
159. Yuan Z.M., Smith P.B., Brundrett R.B., Colvin M., and Fenselau C. Glutathione conjugation with phosphoramide mustard and cyclophosphamide. A mechanistic study using tandem mass spectrometry. Drug Metab Dispos 19 (1991) 625-629
160. Dirven H.A., Megens L., Oudshoorn M.J., Dingemanse M.A., van Ommen B., and van Bladeren P.J. Glutathione conjugation of the cytostatic drug ifosfamide and the role of human glutathione S-transferases. Chem Res Toxicol 8 (1995) 979-986
161. Ishikawa T., and Ali-Osman F. Glutathione-associated cis-diamminedichloroplatinum(II) metabolism and ATP-dependent efflux from leukemia cells. Molecular characterization of glutathione-platinum complex and its biological significance. J Biol Chem 268 (1993) 20116-20125
162. Jensen D.E., and Stelman G.J. Evidence for cytosolic glutathione transferase-mediated denitrosation of nitrosocimetidine and 1-methyl-2-nitro-1-nitrosoguanidine. Carcinogenesis 8 (1987) 1791-1800
163. Buller A.L., Clapper M.L., and Tew K.D. Glutathione S-transferases in nitrogen mustard-resistant and -sensitive cell lines. Mol Pharmacol 31 (1987) 575-578
164. Berhane K., Widersten M., Engstrom A., Kozarich J.W., and Mannervik B. Detoxication of base propenals and other alpha, beta-unsaturated aldehyde products of radical reactions and lipid peroxidation by human glutathione transferases. Proc Natl Acad Sci USA 91 (1994) 1480-1484
165. Gibbs J.P., Czerwinski M., and Slattery J.T. Busulfan-glutathione conjugation catalyzed by human liver cytosolic glutathione S-transferases. Cancer Res 56 (1996) 3678-3681
166. Madan A., Graham R.A., Carroll K.M., Mudra D.R., Burton L.A., Krueger L.A., et al. Effects of prototypical microsomal enzyme inducers on cytochrome P450 expression in cultured human hepatocytes. Drug Metab Dispos 31 (2003) 421-431
167. Dirven H.A., Dictus E.L., Broeders N.L., van Ommen B., and van Bladeren P.J. The role of human glutathione S-transferase isoenzymes in the formation of glutathione conjugates of the alkylating cytostatic drug thiotepa. Cancer Res 55 (1995) 1701-1706
168. Berhane K., and Mannervik B. Inactivation of the genotoxic aldehyde acrolein by human glutathione transferases of classes alpha, mu, and pi. Mol Pharmacol 37 (1990) 251-254
169. Smith M.T., Evans C.G., Doane-Setzer P., Castro V.M., Tahir M.K., and Mannervik B. Denitrosation of 1,3-bis(2-chloroethyl)-1-nitrosourea by class mu glutathione transferases and its role in cellular resistance in rat brain tumor cells. Cancer Res 49 (1989) 2621-2625
170. Ahokas J.T., Davies C., Ravenscroft P.J., and Emmerson B.T. Inhibition of soluble glutathione S-transferase by diuretic drugs. Biochem Pharmacol 33 (1984) 1929-1932
171. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu Rev Pharmacol Toxicol 45 (2005) 51-88
172. Ethell B.T., Beaumont K., Rance D.J., and Burchell B. Use of cloned and expressed human UDP-glucuronosyltransferases for the assessment of human drug conjugation and identification of potential drug interactions. Drug Metab Dispos 29 (2001) 48-53
173. Iyer L., King C.D., Whitington P.F., Green M.D., Roy S.K., Tephly T.R., et al. Genetic predisposition to the metabolism of irinotecan (CPT-11). Role of uridine diphosphate glucuronosyltransferase isoform 1A1 in the glucuronidation of its active metabolite (SN-38) in human liver microsomes. J Clin Invest 101 (1998) 847-854
174. Takeda S., Ishii Y., Iwanaga M., Mackenzie P.I., Nagata K., Yamazoe Y., et al. Modulation of UDP-glucuronosyltransferase function by cytochrome P450: evidence for the alteration of UGT2B7-catalyzed glucuronidation of morphine by CYP3A4. Mol Pharmacol 67 (2005) 665-672
175. Wen Z., Tallman M.N., Ali S.Y., and Smith P.C. UDP-glucuronosyltransferase 1A1 is the principal enzyme responsible for etoposide glucuronidation in human liver and intestinal microsomes: structural characterization of phenolic and alcoholic glucuronides of etoposide and estimation of enzyme kinetics. Drug Metab Dispos 35 (2007) 371-380
176. Watanabe Y., Nakajima M., Ohashi N., Kume T., and Yokoi T. Glucuronidation of etoposide in human liver microsomes is specifically catalyzed by UDP-glucuronosyltransferase 1A1. Drug Metab Dispos 31 (2003) 589-595
177. Sun D., Sharma A.K., Dellinger R.W., Blevins-Primeau A.S., Balliet R.M., Chen G., et al. Glucuronidation of active tamoxifen metabolites by the human UDP glucuronosyltransferases. Drug Metab Dispos 35 (2007) 2006-2014
178. Kaku T., Ogura K., Nishiyama T., Ohnuma T., Muro K., and Hiratsuka A. Quaternary ammonium-linked glucuronidation of tamoxifen by human liver microsomes and UDP-glucuronosyltransferase 1A4. Biochem Pharmacol 67 (2004) 2093-2102
179. Brandon E.F., Sparidans R.W., Meijerman I., Manzanares I., Beijnen J.H., and Schellens J.H. In vitro characterization of the biotransformation of thiocoraline, a novel marine anti-cancer drug. Invest New Drugs 22 (2004) 241-251