Influence of multidrug resistance and drug transport proteins on chemotherapy drug metabolism

Expert Opinion on Drug Metabolism and Toxicology

Volumn 11, Issue 5, 2015, Pages 795-809

  Joyce, Helena ^a,b   McCann, Andrew ^a   Clynes, Martin ^a   Larkin, Annemarie ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b C/o NICB   (Ireland)

Author keywords

ATP binding cassette transporters; Cancer; Chemotherapy drug metabolism; Cytochrome P450; Folate efflux; Glucuronidation; Glutathione S transferase conjugates; Multidrug resistance; Solute carrier transporters

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; BREAST CANCER RESISTANCE PROTEIN; CYTOCHROME P450; CYTOCHROME P450 3A4; CYTOTOXIC AGENT; DRUG METABOLIZING ENZYME; FOLIC ACID; GLUCURONIC ACID; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 5; OXIDOREDUCTASE; SULFATE; XENOBIOTIC AGENT; CARRIER PROTEIN;

CANCER CHEMOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; DISEASE COURSE; DRUG METABOLISM; DRUG RESISTANCE; DRUG TRANSPORT; DRUG UPTAKE; GLUCURONIDATION; HUMAN; METASTASIS; MULTIDRUG RESISTANCE; OUTER MEMBRANE; PHENOTYPE; PROTEIN FAMILY; REVIEW; THERAPY; ANIMAL; METABOLISM; NEOPLASMS; PATHOLOGY; RECURRENT DISEASE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; DISEASE PROGRESSION; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; MEMBRANE TRANSPORT PROTEINS; NEOPLASM METASTASIS; NEOPLASMS; RECURRENCE;

EID: 84928898540     PISSN: 17425255     EISSN: 17447607     Source Type: Journal    
DOI: 10.1517/17425255.2015.1028356     Document Type: Review

References (161)

1. Gillet JP, Gottesman MM. Mechanisms of multidrug resistance in cancer. Methods Mol Biol 2010;596:47-76
2. Clynes M. Multiple drug resistance in cancer 2: molecular, cellular and clinical aspects. Springer; Netherlands: 2010
3. Heenan M, O'Driscoll L, Cleary I, et al. Isolation from a human MDR lung cell line of multiple clonal subpopulations which exhibit significantly different drug resistance. Int J Cancer 1997;71(5):907-15
4. Liang Y, O'Driscoll L, McDonnell S, et al. Enhanced in vitro invasiveness and drug resistance with altered gene expression patterns in a human lung carcinoma cell line after pulse selection with anticancer drugs. Int J Cancer 2004;111(4):484-93
5. Giacomini KM, Huang SM, Tweedie DJ, et al. Membrane transporters in drug development. Nat Rev Drug Discov 2010;9(3):215-36
6. Hediger MA, Romero MF, Peng JB, et al. The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteinsIntroduction. Pflugers Arch 2004;447(5):465-8
7. Shugarts S, Benet LZ. The role of transporters in the pharmacokinetics of orally administered drugs. Pharm Res 2009;26(9):2039-54
8. Vadlapatla RK, Vadlapudi AD, Pal D, Mitra AK. Mechanisms of drug resistance in cancer chemotherapy: coordinated role and regulation of efflux transporters and metabolizing enzymes. Curr Pharm Des 2013;19(40):7126-40
9. Urquhart BL, Tirona RG, Kim RB. Nuclear receptors and the regulation of drug-metabolizing enzymes and drug transporters: implications for interindividual variability in response to drugs. J Clin Pharmacol 2007;47(5):566-78
10. Chen Y, Tang Y, Guo C, et al. Nuclear receptors in the multidrug resistance through the regulation of drugmetabolizing enzymes and drug transporters. Biochem Pharmacol 2012;83(8):1112-26
11. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011;11(2):85-95
12. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012;21(3):297-308
13. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis 2013;4:e532
14. Dobson PD, Kell DB. Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule Nat Rev Drug Discov 2008;7(3):205-20
15. Sprowl JA, Mikkelsen TS, Giovinazzo H, Sparreboom A. Contribution of tumoral and host solute carriers to clinical drug response. Drug Resist Updat 2012;15(1-2):5-20
16. Assaraf YG. Molecular basis of antifolate resistance. Cancer Metastasis Rev 2007;26(1):153-81
17. Farrell JJ, Elsaleh H, Garcia M, et al. Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 2009;136(1):187-95
18. Okabe M, Szakacs G, Reimers MA, et al. Profiling SLCO and SLC22 genes in the NCI-60 cancer cell lines to identify drug uptake transporters. Mol Cancer Ther 2008;7(9):3081-91
19. Cordon-Cardo C, O'Brien JP, Boccia J, et al. Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues. J Histochem Cytochem 1990;38(9):1277-87
20. Gottesman MM, Ludwig J, Xia D, Szakacs G. Defeating drug resistance in cancer. Discov Med 2006;6(31):18-23
21. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003;55(1):3-29.
22. Jones PM, George AM. The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 2004;61(6):682-99
23. Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Hum Genomics 2009;3(3):281-90
24. Schinkel AH, Kemp S, Dolle M, et al. N-glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J Biol Chem 1993;268(10):7474-81
25. Biedler JL, Riehm H. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenetic studies. Cancer Res 1970;30(4):1174-84
26. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976;455(1):152-62
27. Riehm H, Biedler JL. Cellular resistance to daunomycin in Chinese hamster cells in vitro. Cancer Res 1971;31(4):409-12
28. Dano K. Cross resistance between vinca alkaloids and anthracyclines in Ehrlich ascites tumor in vivo. Cancer Chemother Rep 1972;56(6):701-8
29. Dano K. Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim Biophys Acta 1973;323(3):466-83
30. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993;62:385-427
31. Bellamy WT. P-glycoproteins and multidrug resistance. Annu Rev Pharmacol Toxicol 1996;36:161-83
32. Wang Z, Chen Y, Liang H, et al. P-glycoprotein substrate models using support vector machines based on a comprehensive data set. J Chem Inf Model 2011;51(6):1447-56
33. Chen L, Li Y, Yu H, et al. Computational models for predicting substrates or inhibitors of P-glycoprotein. Drug Discov Today 2012;17(7-8):343-51
34. Wang XK, Fu LW. Interaction of tyrosine kinase inhibitors with the MDRrelated ABC transporter proteins. Curr Drug Metab 2010;11(7):618-28
35. Hegedus T, Orfi L, Seprodi A, et al. Interaction of tyrosine kinase inhibitors with the human multidrug transporter proteins, MDR1 and MRP1. Biochim Biophys Acta 2002;1587(2-3):318-25
36. Greer DA, Ivey S. Distinct N-glycan glycosylation of P-glycoprotein isolated from the human uterine sarcoma cell line MES-SA/Dx5. Biochim Biophys Acta 2007;1770(9):1275-82
37. Allen JD, Brinkhuis RF, Wijnholds J, Schinkel AH. The mouse Bcrp1/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res 1999;59(17):4237-41
38. Loo TW, Clarke DM. Quality control by proteases in the endoplasmic reticulum. Removal of a proteasesensitive site enhances expression of human P-glycoprotein. J Biol Chem 1998;273(49):32373-6
39. Ambudkar SV, Dey S, Hrycyna CA, et al. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 1999;39:361-98
40. Breier A, Gibalova L, Seres M, et al. New insight into p-glycoprotein as a drug target. Anticancer Agents Med Chem 2013;13(1):159-70
41. Robertson SJ, Kania KD, Hladky SB, Barrand MA. P-glycoprotein expression in immortalised rat brain endothelial cells: comparisons following exogenously applied hydrogen peroxide and after hypoxia-reoxygenation. J Neurochem 2009;111(1):132-41
42. 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):15665-70
43. Allikmets R, Schriml LM, Hutchinson A, et al. A human placenta-specific ATPbinding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 1998;58(23):5337-9
44. Miyake K, Mickley L, Litman T, et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantroneresistant cells: demonstration of homology to ABC transport genes. Cancer Res 1999;59(1):8-13
45. Kage K, Tsukahara S, Sugiyama T, et al. Dominant-negative inhibition of breast cancer resistance protein as drug efflux pump through the inhibition of S-S dependent homodimerization. Int J Cancer 2002;97(5):626-30
46. Ozvegy C, Litman T, Szakacs G, et al. Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem Biophys Res Commun 2001;285(1):111-17
47. Mo W, Zhang JT. Human ABCG2: structure, function, and its role in multidrug resistance. Int J Biochem Mol Biol 2012;3(1):1-27
48. Natarajan K, Xie Y, Baer MR, Ross DD. Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance. Biochem Pharmacol 2012;83(8):1084-103
49. Ebert B, Seidel A, Lampen A. Identification of BCRP as transporter of benzo[a]pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists. Carcinogenesis 2005;26(10):1754-63
50. Turner JG, Gump JL, Zhang C, et al. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood 2006;108(12):3881-9
51. Wang XQ, Ongkeko WM, Chen L, et al. Octamer 4 (Oct4) mediates chemotherapeutic drug resistance in liver cancer cells through a potential Oct4-AKT-ATP-binding cassette G2 pathway. Hepatology 2010;52(2):528-39
52. Benderra Z, Faussat AM, Sayada L, et al. Breast cancer resistance protein and P-glycoprotein in 149 adult acute myeloid leukemias. Clin Cancer Res 2004;10(23):7896-902
53. Krishnamurthy P, Ross DD, Nakanishi T, et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004;279(23):24218-25
54. Bailey-Dell KJ, Hassel B, Doyle LA, Ross DD. Promoter characterization and genomic organization of the human breast cancer resistance protein (ATPbinding cassette transporter G2) gene. Biochim Biophys Acta 2001;1520(3):234-41
55. Honjo Y, Morisaki K, Huff LM, et al. Single-nucleotide polymorphism (SNP) analysis in the ABC half-transporter ABCG2 (MXR/BCRP/ABCP1). Cancer Biol Ther 2002;1(6):696-702
56. Nakanishi T, Karp JE, Tan M, et al. Quantitative analysis of breast cancer resistance protein and cellular resistance to flavopiridol in acute leukemia patients. Clin Cancer Res 2003;9(9):3320-8
57. SuVannasankha A, Minderman H, O'Loughlin KL, et al. Breast cancer resistance protein (BCRP/MXR/ABCG2) in adult acute lymphoblastic leukaemia: frequent expression and possible correlation with shorter disease-free survival. Br J Haematol 2004;127(4):392-8
58. SuVannasankha A, Minderman H, O'Loughlin KL, et al. Breast cancer resistance protein (BCRP/MXR/ABCG2) in acute myeloid leukemia: discordance between expression and function. Leukemia 2004;18(7):1252-7
59. Ozvegy C, Varadi A, Sarkadi B. Characterization of drug transport, ATP hydrolysis, and nucleotide trapping by the human ABCG2 multidrug transporter. Modulation of substrate specificity by a point mutation. J Biol Chem 2002;277(50):47980-90
60. Volk EL, Rohde K, Rhee M, et al. Methotrexate cross-resistance in a mitoxantrone-selected multidrug-resistant MCF7 breast cancer cell line is attributable to enhanced energydependent drug efflux. Cancer Res 2000;60(13):3514-21
61. Volk EL, Farley KM, Wu Y, et al. Overexpression of wild-type breast cancer resistance protein mediates methotrexate resistance. Cancer Res 2002;62(17):5035-40
62. Cole SP, Deeley RG. Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 2006;27(8):438-46
63. Leslie EM, Deeley RG, Cole SP. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 2005;204(3):216-37
64. Kool M, de Haas M, Scheffer GL, et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistanceassociated protein gene (MRP1), in human cancer cell lines. Cancer Res 1997;57(16):3537-47
65. Wada M, Toh S, Taniguchi K, et al. Mutations in the canilicular multispecific organic anion transporter (cMOAT) gene, a novel ABC transporter, in patients with hyperbilirubinemia II/Dubin-Johnson syndrome. Hum Mol Genet 1998;7(2):203-7
66. Van Kuijck MA, Kool M, Merkx GF, et al. Assignment of the canalicular multispecific organic anion transporter gene (CMOAT) to human chromosome 10q24 and mouse chromosome 19D2 by fluorescent in situ hybridization. Cytogenet Cell Genet 1997;77(3-4):285-7
67. Borst P, Zelcer N, Van de Wetering K. MRP2 and 3 in health and disease. Cancer Lett 2006;234(1):51-61
68. Jedlitschky G, Hoffmann U, Kroemer HK. Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Expert Opin Drug Metab Toxicol 2006;2(3):351-66
69. Trauner M, Boyer JL. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 2003;83(2):633-71
70. 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):1310-19
71. Cui Y, Konig J, Buchholz JK, et al. 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):929-37
72. Keppler D, Konig J. Hepatic canalicular membrane 5: expression and localization of the conjugate export pump encoded by the MRP2 (cMRP/cMOAT) gene in liver. Faseb J 1997;11(7):509-16
73. Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 2000;92(16):1295-302
74. 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):1219-28
75. Materna V, Liedert B, Thomale J, Lage H. Protection of platinum-DNA adduct formation and reversal of cisplatin resistance by anti-MRP2 hammerhead ribozymes in human cancer cells. Int J Cancer 2005;115(3):393-402
76. Liedert B, Materna V, Schadendorf D, et al. 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 2003;121(1):172-6
77. Taniguchi K, Wada M, Kohno K, et al. A human canalicular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation. Cancer Res 1996;56(18):4124-9
78. 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):5475-9
79. Materna V, Stege A, Surowiak P, et al. RNA interference-triggered reversal of ABCC2-dependent cisplatin resistance in human cancer cells. Biochem Biophys Res Commun 2006;348(1):153-7
80. Ma JJ, Chen BL, Xin XY. Inhibition of multi-drug resistance of ovarian carcinoma by small interfering RNA targeting to MRP2 gene. Arch Gynecol Obstet 2009;279(2):149-57
81. Kobayashi K, Ito K, Takada T, et al. Functional analysis of nonsynonymous single nucleotide polymorphism type ATP-binding cassette transmembrane transporter subfamily C member 3. Pharmacogenet Genomics 2008;18(9):823-33
82. Zhou SF, Wang LL, Di YM, et al. Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 2008;15(20):1981-2039
83. Kool M, Van der Linden M, de Haas M, et al. MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 1999;96(12):6914-19
84. Zelcer N, Saeki T, Reid G, et al. Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 2001;276(49):46400-7
85. Partanen L, Staaf J, Tanner M, et al. Amplification and overexpression of the ABCC3 (MRP3) gene in primary breast cancer. Genes Chromosomes Cancer 2012;51(9):832-40
86. Zhao Y, Lu H, Yan A, et al. ABCC3 as a marker for multidrug resistance in nonsmall cell lung cancer. Sci Rep 2013;3:3120
87. Guengerich FP. Cytochrome P450s and other enzymes in drug metabolism and toxicity. Aaps J 2006;8(1):E101-11
88. Van Herwaarden AE, Van Waterschoot RA, Schinkel AH. How important is intestinal cytochrome P4503 A metabolism Trends Pharmacol Sci 2009;30(5):223-7
89. McFadyen MC, Melvin WT, Murray GI. Cytochrome P450 enzymes: novel options for cancer therapeutics. Mol Cancer Ther 2004;3(3):363-71
90. Sim SC, Ingelman-Sundberg M. The Human Cytochrome P450 (CYP) Allele Nomenclature website: a peer-reviewed database of CYP variants and their associated effects. Hum Genomics 2010;4(4):278-81
91. Rodriguez-Antona C, Ingelman-Sundberg M. Cytochrome P450 pharmacogenetics and cancer. Oncogene 2006;25(11):1679-91
92. Engels FK, Ten Tije AJ, Baker SD, et al. Effect of cytochrome P450 3A4 inhibition on the pharmacokinetics of docetaxel. Clin Pharmacol Ther 2004;75(5):448-54
93. Desta Z, Ward BA, Soukhova NV, Flockhart DA. Comprehensive evaluation of tamoxifen sequential biotransformation by the human cytochrome P450 system in vitro: prominent roles for CYP3A and CYP2D6. J Pharmacol Exp Ther 2004;310(3):1062-75
94. Schellens JH, Malingre MM, Kruijtzer CM, et al. Modulation of oral bioavailability of anticancer drugs: from mouse to man. Eur J Pharm Sci 2000;12(2):103-10
95. Azzariti A, Porcelli L, Quatrale AE, et al. The coordinated role of CYP450 enzymes and P-gp in determining cancer resistance to chemotherapy. Curr Drug Metab 2011;12(8):713-21
96. Van Waterschoot RA, Schinkel AH. A critical analysis of the interplay between cytochrome P450 3A and P-glycoprotein: recent insights from knockout and transgenic mice. Pharmacol Rev 2011. 63. 2. 390-410
97. Hendrikx JJ, Lagas JS, Rosing H, et al. P-glycoprotein and cytochrome P450 3A act together in restricting the oral bioavailability of paclitaxel. Int J Cancer 2013;132(10):2439-47
98. Jibodh RA, Lagas JS, Nuijen B, et al. Taxanes: old drugs, new oral formulations. Eur J Pharmacol 2013;717(1-3):40-6
99. Joerger M. Metabolism of the taxanes including nab-paclitaxel. Expert Opin Drug Metab Toxicol 2014;14:1-12
100. Gligorov J, Lotz JP. Preclinical pharmacology of the taxanes: implications of the differences. Oncologist 2004;9(Suppl 2):3-8
101. Lagas JS, Vlaming ML, Van Tellingen O, et al. Multidrug resistance protein 2 is an important determinant of paclitaxel pharmacokinetics. Clin Cancer Res 2006;12(20 Pt 1):6125-32
102. Sparreboom A, Van Asperen J, Mayer U, et al. Limited oral bioavailability and active epithelial excretion of paclitaxel (Taxol) caused by P-glycoprotein in the intestine. Proc Natl Acad Sci USA 1997;94(5):2031-5
103. Hopper-Borge EA, Churchill T, Paulose C, et al. Contribution of Abcc10 (Mrp7) to in vivo paclitaxel resistance as assessed in Abcc10(-/-) mice. Cancer Res 2011;71(10):3649-57
104. Meijerman I, Beijnen JH, Schellens JH. Combined action and regulation of phase II enzymes and multidrug resistance proteins in multidrug resistance in cancer. Cancer Treat Rev 2008;34(6):505-20
105. Harmsen S, Meijerman I, Beijnen JH, Schellens JH. The role of nuclear receptors in pharmacokinetic drug-drug interactions in oncology. Cancer Treat Rev 2007;33(4):369-80
106. Cerveny L, Svecova L, Anzenbacherova E, et al. Valproic acid induces CYP3A4 and MDR1 gene expression by activation of constitutive androstane receptor and pregnane X receptor pathways. Drug Metab Dispos 2007;35(7):1032-41
107. Handschin C, Meyer UA. Induction of drug metabolism: the role of nuclear receptors. Pharmacol Rev 2003;55(4):649-73
108. Tolson AH, Wang H. Regulation of drug-metabolizing enzymes by xenobiotic receptors: PXR and CAR. Adv Drug Deliv Rev 2010;62(13):1238-49
109. Ballatori N, Krance SM, Notenboom S, et al. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 2009;390(3):191-214
110. Valko M, Leibfritz D, Moncol J, et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39(1):44-84
111. Shanker M, Willcutts D, Roth JA, Ramesh R. Drug resistance in lung cancer. Lung Cancer: Targets and Therapy 2010;1:23-6
112. Townsend DM, Tew KD. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 2003;22(47):7369-75
113. Burg D, Mulder GJ. Glutathione conjugates and their synthetic derivatives as inhibitors of glutathione-dependent enzymes involved in cancer and drug resistance. Drug Metab Rev 2002;34(4):821-63
114. Homolya L, Varadi A, Sarkadi B. Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 2003;17(1-4):103-14
115. Leslie EM, Haimeur A, Waalkes MP. Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J Biol Chem 2004;279(31):32700-8
116. Bodo A, Bakos E, Szeri F, et al. The role of multidrug transporters in drug availability, metabolism and toxicity. Toxicol Lett 2003;140-141:133-43
117. 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(22):5130-6
118. 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(23):5232-7
119. Ciaccio PJ, Shen H, Kruh GD, Tew KD. Effects of chronic ethacrynic acid exposure on glutathione conjugation and MRP expression in human colon tumor cells. Biochem Biophys Res Commun 1996;222(1):111-15
120. Taguchi Y, Yoshida A, Takada Y, et al. Anti-cancer drugs and glutathione stimulate Vanadate-induced trapping of nucleotide in multidrug resistanceassociated protein (MRP). FEBS Lett 1997;401(1):11-14
121. Morrow CS, Smitherman PK, Diah SK, et al. 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(32):20114-20
122. Barnouin K, Leier I, Jedlitschky G, et al. Multidrug resistance protein-mediated transport of chlorambucil and melphalan conjugated to glutathione. Br J Cancer 1998;77(2):201-9
123. Yamasaki M, Makino T, Masuzawa T, et al. Role of multidrug resistance protein 2 (MRP2) in chemoresistance and clinical outcome in oesophageal squamous cell carcinoma. Br J Cancer 2011;104(4):707-13
124. Ozols RF. Pharmacologic reversal of drug resistance in ovarian cancer. Semin Oncol 1985;12(3 Suppl 4):7-11
125. Traverso N, Ricciarelli R, Nitti M, et al. Role of glutathione in cancer progression and chemoresistance. Oxid Med Cell Longev 2013;2013:10
126. Oguri T, Fujiwara Y, Isobe T, et al. Expression of gamma-glutamylcysteine synthetase (gamma-GCS) and multidrug resistance-associated protein (MRP), but not human canalicular multispecific organic anion transporter (cMOAT), genes correlates with exposure of human lung cancers to platinum drugs. Br J Cancer 1998;77(7):1089-96
127. Gonen N, Assaraf YG. Antifolates in cancer therapy: structure, activity and mechanisms of drug resistance. Drug Resist Updat 2012;15(4):183-210
128. Picciano MF, Stokstad ELR, Gregory JF, et al. Contemporary Issues in Clinical Nutrition, vol 13, Folic Acid Metabolism in Health and Disease. New York: Wiley-Liss, 1990:1-12
129. Assaraf YG. The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist Updat 2006;9(4-5):227-46
130. Masuda M, I'Izuka Y, Yamazaki M, et al. Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats. Cancer Res 1997;57(16):3506-10
131. Hooijberg JH, Broxterman HJ, Kool M, et al. Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 1999;59(11):2532-5
132. Zeng H, Chen ZS, Belinsky MG, et al. Transport of methotrexate (MTX) and folates by multidrug resistance protein (MRP) 3 and MRP1: effect of polyglutamylation on MTX transport. Cancer Res 2001;61(19):7225-32
133. Chen ZS, Lee K, Walther S, et al. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 2002;62(11):3144-50
134. Shafran A, Ifergan I, Bram E, et al. ABCG2 harboring the Gly482 mutation confers high-level resistance to various hydrophilic antifolates. Cancer Res 2005;65(18):8414-22
135. Kusuhara H, Han YH, Shimoda M, et al. Reduced folate derivatives are endogenous substrates for cMOAT in rats. Am J Physiol 1998;275(4 Pt 1):G789-96
136. Mackenzie PI, Bock KW, Burchell B, et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 2005;15(10):677-85
137. Tukey RH, Strassburg CP. Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Annu Rev Pharmacol Toxicol 2000;40:581-616
138. Nagar S, Remmel RP. Uridine diphosphoglucuronosyltransferase pharmacogenetics and cancer. Oncogene 2006;25(11):1659-72
139. Lazarus P, Sun D. Potential role of UGT pharmacogenetics in cancer treatment and prevention: focus on tamoxifen and aromatase inhibitors. Drug Metab Rev 2010;42(1):182-94
140. Starlard-Davenport A, Lyn-Cook B, Beland FA, Pogribny IP. The role of UDP-glucuronosyltransferases and drug transporters in breast cancer drug resistance. Exp Oncol 2010;32(3):172-80
141. Li J, Bluth MH. Pharmacogenomics of drug metabolizing enzymes and transporters: implications for cancer therapy. Pharmgenomics Pers Med 2011;4:11-33
142. Rivory LP, Riou JF, Haaz MC, et al. Identification and properties of a major plasma metabolite of irinotecan (CPT-11) isolated from the plasma of patients. Cancer Res 1996;56(16):3689-94
143. Dodds HM, Haaz MC, Riou JF, et al. Identification of a new metabolite of CPT-11 (irinotecan): pharmacological properties and activation to SN-38. J Pharmacol Exp Ther 1998;286(1):578-83
144. Sugiyama Y, Kato Y, Chu X. Multiplicity of biliary excretion mechanisms for the camptothecin derivative irinotecan (CPT-11), its metabolite SN-38, and its glucuronide: role of canalicular multispecific organic anion transporter and P-glycoprotein. Cancer Chemother Pharmacol 1998;42(Suppl):S44-9
145. Chu XY, Kato Y, Ueda K, et al. Biliary excretion mechanism of CPT-11 and its metabolites in humans: involvement of primary active transporters. Cancer Res 1998;58(22):5137-43
146. Iyer L, Das S, Janisch L, et al. UGT1A1∗28 polymorphism as a determinant of irinotecan disposition and toxicity. Pharmacogenomics J 2002;2(1):43-7
147. Fredriksson R, Nordstrom KJ, Stephansson O, et al. The solute carrier (SLC) complement of the human genome: phylogenetic classification reveals four major families. FEBS Lett 2008;582(27):3811-16
148. Russel FM. Transporters: importance in drug absorption, distribution, and removal. In: Pang KS, Rodrigues AD, Peter RM, editos Enzyme-and transporter-based drug-drug interactions. Springer; New York: 2010. p. 27-49
149. Masereeuw R, Russel FG. Therapeutic implications of renal anionic drug transporters. Pharmacol Ther 2010;126(2):200-16
150. Galmarini CM, Mackey JR, Dumontet C. Nucleoside analogues: mechanisms of drug resistance and reversal strategies. Leukemia 2001;15(6):875-90
151. Mackey JR, Baldwin SA, Young JD, Cass CE. Nucleoside transport and its significance for anticancer drug resistance. Drug Resist Updat 1998;1(5):310-24
152. Cascorbi I. Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacol Ther 2006;112(2):457-73.
153. Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm 2011;8(6):1996-2011
154. Sharom FJ. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 2008;9(1):105-27
155. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2(1):48-58
156. Gillet JP, Efferth T, Remacle J. Chemotherapy-induced resistance by ATP-binding cassette transporter genes. Biochim Biophys Acta 2007;1775(2):237-62
157. Kruh GD, Belinsky MG. The MRP family of drug efflux pumps. Oncogene 2003;22(47):7537-52
158. 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(1):21-53
159. Konig J, Nies AT, Cui Y, et al. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1999;1461(2):377-94
160. Mao Q, Unadkat JD. Role of the breast cancer resistance protein (ABCG2) in drug transport. Aaps J 2005;7(1):E118-33
161. Takara K, Sakaeda T, Okumura K. An update on overcoming MDR1-mediated multidrug resistance in cancer chemotherapy. Curr Pharm Des 2006;12(3):273-86