Multidrug resistance proteins (MRPs) and implication in drug development

Drug Development Research

Volumn 64, Issue 1, 2005, Pages 1-18

  Tian, Quan ^a   Zhang, Jing ^a   Chan, Eli ^a   Duan, Wei ^b   Zhou, Shufeng ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Drug development; Drug transport; MRP; Pharmacokinetics; Polymorphism; Toxicity

Indexed keywords

5 (4,6 DIMETHYL 1,3,2 DIOXAPHOSPHORINAN 2 YL) 2,6 DIMETHYL 4 (3 NITROPHENYL) 3 PYRIDINECARBOXYLIC ACID 2 (4 BENZHYDRYL 1 PIPERAZINYL)ETHYL ESTER P OXIDE; 7 ETHYL 10 HYDROXYCAMPTOTHECIN; ABC TRANSPORTER; ANTHRACYCLINE; ANTIANDROGEN; ANTINEOPLASTIC AGENT; ANTISENSE OLIGONUCLEOTIDE; APIGENIN; B 22956; BENZBROMARONE; CAMPTOTHECIN; CELECOXIB; CHLORAMBUCIL; CHLORMETHINE; CISPLATIN; CYCLOOXYGENASE 2 INHIBITOR; CYCLOPHOSPHAMIDE; CYCLOSPORIN; DACTINOMYCIN; DAUNORUBICIN; DICLOFENAC; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; ENZYME INHIBITOR; ESTRAMUSTINE; ESTROGEN; ETACRYNIC ACID; ETOPOSIDE; FLUTAMIDE; FUROSEMIDE; GADOLINIUM CHELATE; GANCICLOVIR; GENISTEIN; GLIBENCLAMIDE; HYDROXYFLUTAMIDE; INDOMETACIN; IRINOTECAN; ISIS 7597; ISOXAZOLE DERIVATIVE; LY 402913; LY 475776; MELPHALAN; MERCAPTOPURINE; METHOTREXATE; METHOXY ISOBUTYL ISONITRILE TECHNETIUM TC 99M; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; MULTIDRUG RESISTANCE PROTEIN 7; MULTIDRUG RESISTANCE PROTEIN 8; MULTIDRUG RESISTANCE PROTEIN 9; NUCLEOSIDE DERIVATIVE; PACLITAXEL; PARACETAMOL; PRANLUKAST; PROBENECID; PROGESTERONE; PROTEINASE INHIBITOR; QUERCETIN; RALTITREXED; RITONAVIR; ROFECOXIB; SAQUINAVIR; STEROID; SULFINPYRAZONE; SULFONYLUREA; TENIPOSIDE; TETROFOSMIN TC 99M; THIOTEPA; TIOGUANINE; TOPOTECAN; UNCLASSIFIED DRUG; VERAPAMIL; VERLUKAST; VINCA ALKALOID; VINCRISTINE; XENOBIOTIC AGENT; ZIDOVUDINE;

CANCER CHEMOTHERAPY; CELL MEMBRANE; DNA POLYMORPHISM; DRUG ABSORPTION; DRUG DEVELOPMENT; DRUG ELIMINATION; DRUG INTERACTION; DRUG SAFETY; DRUG SYNTHESIS; DRUG TRANSPORT; GENE MUTATION; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; XENOBIOTIC METABOLISM;

EID: 18044376796     PISSN: 02724391     EISSN: None     Source Type: Journal    
DOI: 10.1002/ddr.10427     Document Type: Review

References (198)

1. Adachi M, Sampath J, Lan LB, Sun D, Hargrove P, Flatley R, Tatum A, Edwards MZ, Wezeman M, Matherly L, Drake R, Schuetz J. 2002. Expression of MRP4 confers resistance to ganciclovir and compromises bystander cell killing. J Biol Chem 277:38998-39004.
2. Akimaru K, Kuo MT, Furuta K, Suzuki M, Noyori R, Ishikawa T. 1996. Induction of MRP/GS-X pump and cellular resistance to anticancer prostaglandins. Cytotechnology 19:221-227.
3. Akita H, Suzuki H, Ito K, Kinoshita S, Sato N, Takikawa H, Sugiyama Y. 2001. Characterization of bile acid transport mediated by multidrug resistance associated protein 2 and bile salt export pump. Biochim Biophys Acta 1511:7-16.
4. Altenberg GA. 2004. Structure of multidrug-resistance proteins of the ATP-binding cassette (ABC) superfamily. Curr Med Chem Anti-Cancer Agents 4:53-62.
5. Aoki S, Chen ZS, Higasiyama K, Setiawan A, Akiyama S, Kobayashi M. 2001. Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn J Cancer Res 92:886-895.
6. Assaraf YG, Sierra EE, Babani S, Goldman ID. 1999. Inhibitory effects of prostaglandin Al on membrane transport of folates mediated by both the reduced folate carrier and ATP-driven exporters. Biochem Pharmacol 58:1321-1327.
7. Assaraf YG, Rothem L, Hooijberg JH, Stark M, Ifergan I, Kathmann I, Dijkmans BA, Peters GJ, Jansen G. 2003. Loss of multidrug resistance protein 1 expression and folate efflux activity results in a highly concentrative folate transport in human leukemia cells. J Biol Chem 278:6680-6686.
8. Assem M, Schuetz EG, Leggas M, Sun D, Yasuda K, Reid G, Zelcer N, Adachi M, Strom S, Evans RM, Moore DD, Borst P, Schuetz JD. 2004. Interactions between hepatic Mrp4 and Sult2A as revealed by the constitutive androstane receptor and Mrp4 knockout mice. J Biol Chem 279:22250-22257.
9. Bai J, Lai L, Yeo HC, Goh BC, Tan TM. 2004. Multidrug resistance protein 4 (MRP4/ABCC4) mediates efflux of bimane-glutathione. Int J Biochem Cell Biol 36:247-257.
10. Bakos E, Evers R, Sinko E, Varadi A, Borst P, Sarkadi B. 2000. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol Pharmacol 57:760-768.
11. Bandi N, Kompella UB. 2002. Budesonide reduces multidrug resistance-associated protein 1 expression in an airway epithelial cell line (Calu-1). Eur J Pharmacol 437:9-17.
12. Barnouin K, Leier I, Jedlitschky G, Pourtier-Manzanedo A, Konig J, Lehmann WD, Keppler D. 1998. Multidrug resistance protein-mediated transport of chlorambucil and melphalan conjugated to glutathione. Br J Cancer 77:201-209.
13. Barrand MA, Rhodes T, Center MS, Twentyman PR. 1993. Chemosensitisation and drug accumulation effects of cyclosporin A, PSC-833 and verapamil in human MDR large cell lung cancer cells expressing a 190k membrane protein distinct from P-glycoprotein. Eur J Cancer 29A:408-415.
14. Begley DJ. 2004. ABC transporters and the blood-brain barrier. Curr Pharm Des 10:1295-1312.
15. Belinsky MG, Bain LJ, Balsara BB, Testa JR, Kruh GD. 1998. Characterization of MOAT-C and MOAT-D, new members of the MRP/cMOAT subfamily of transporter proteins. J Natl Cancer Inst 90:1735-1741.
16. Belinsky MG, Chen ZS, Shchaveleva I, Zeng H, Kruh GD. 2002. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 62:6172-6177.
17. Bera TK, Lee S, Salvatore G, Lee B, Pastan I. 2001. MRP8, a new member of ABC transporter superfamily, identified by EST database mining and gene prediction program, is highly expressed in breast cancer. Mol Med 7:509-516.
18. Bera TK IC, Kumar V, Lee S, Lee B, Pastan I. 2002. MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc Natl Acad Sci USA 99:6997-7002.
19. Bodo A, Bakos E, Szeri F, Varadi A, Sarkadi B. 2003. Differential modulation of the human liver conjugate transporters MRP2 and MRP3 by bile acids and organic anions. J Biol Chem 278:23529-23537.
20. Boraldi F, Quaglino D, Croce MA, Garcia Fernandez MI, Tiozzo R, Gheduzzi D, Bacchelli B, Pasquali Ronchetti I. 2003. Multidrug resistance protein-6 (MRP6) in human dermal fibroblasts. Comparison between cells from normal subjects and from Pseudoxanthoma elasticum patients. Matrix Biol 22:491-500.
21. Borst P, Elferink RO. 2002. Mammalian ABC transporters in health and disease. Annu Rev Biochem 71:537-592.
22. Borst P, Evers R, Kool M, Wijnholds J. 1999. The multidrug resistance protein family. Biochim Biophys Acta 1461:347-357.
23. Borst P, Evers R, Kool M, Wijnholds J. 2000. A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92:1295-1302.
24. Buchler M, Konig J, Brom M, Kartenbeck J, Spring H, Horie T, Keppler D. 1996. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMRP, reveals a novel conjungate export pump deficient in hyperbilirubinemic rats. J Biol Chem 271:15091-15098.
25. Burger H, Nooter K, Zaman GJ, Sonneveld P, van Wingerden KE, Oostrum RG, Stoter G. 1994. Expression of the multidrug resistance-associated protein (MRP) in acute and chronic leukemias. Leukemia 8:990-997.
26. Cai L, Lumsden A, Guenther UP, Neidner SA, Zach S, Knoblauch H, Ramesar R, Hohl D, Gallen DF, Neidner KH, Lindpaintner K, Richards RI, Struk B. 2001. A novel Q378X mutation exists in the transmembrane transporter protein ABCC6 and its pseudogene: implications for mutation analysis in pseudoxanthoma elasticum. J Mol Med 79:536-546.
27. Chan LM, Lowes S, Hirst BH. 2004. The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur J Pharm Sci 21:25-51.
28. Chassaing N, Martin L, Mazereeuw J, Barrie L, Nizard S, Bonafe JL, Calvas P, Hovnanian A. 2004. Novel ABCC6 mutations in pseudoxanthoma elasticum. J Invest Dermatol 122:608-613.
29. Chen LM, Wu XP, Ruan JW, Liang YJ, Ding Y, Shi Z, Wang XW, Gu LQ, Fu LW. 2004. Screening novel, potent multidrug-resistant modulators from imidazole derivatives. Oncol Res 14:355-362.
30. Chen WS, Luker KE, Dahlheimer JL, Pica CM, Luker GD, Piwnica-Worms D. 2000. Effects of MDR1 and MDR3 P-glycoproteins, MRP1, and BCRP/MXR/ABCP on the transport of (99m)Tc-tetrofosmin. Biochem Pharmacol 60:413-426.
31. Chen ZS, Lee K, Kruh GD. 2001. Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 276:33747-33754.
32. Chen ZS, Lee K, Walther S, Raftogianis RB, Kuwano M, Zeng H, Kruh GD. 2002. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 62:3144-3150.
33. Chen ZS, Hopper-Borge E, Belinsky MG, Shchaveleva I, Kotova E, Kruh GD. 2003. Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 63:351-358.
34. Chu XY, Suzuki H, Ueda K, Kato Y, Akiyama S, Sugiyama Y. 1999. Active efflux of CPT-11 and its metabolites in human KB-derived cell lines. J Pharmacol Exp Ther 288:735-741.
35. Chu XY, Huskey SE, Braun MP, Sarkadi B, Evans DC, 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.
36. Cole SP, Downes HF, Mirski SE, Clements DJ. 1990. Alterations in glutathione and glutathione-related enzymes in a multidrug-resistant small cell lung cancer cell line. Mol Pharmacol 37:192-197.
37. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG. 1992. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650-1654.
38. Cole SP, Sparks KE, Fraser K, Loe DW, Grant CE, Wilson GM, Deeley RG. 1994. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54:5902-5910.
39. Conrad S, Kauffmann HM, Ito K, Deeley RG, Cole SP, Schrenk D. 2001. Identification of human multidrug resistance protein 1 (MRP1) mutations and characterization of a G671V substitution. J Hum Genet 46:656-663.
40. Conrad S, Kauffmann HM, Ito K, Leslie EM, Deeley RG, Schrenk D, Cole SP. 2002. A naturally occurring mutation in MRP1 results in a selective decrease in organic anion transport and in increased doxorubicin resistance. Pharmacogenetics 12:321-330.
41. Cui Y, Konig J, Buchholz JK, Spring H, Leier I, Keppler D. 1999. Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 55:929-937.
42. Dallas S, Ronaldson PT, Bendayan M, Bendayan R. 2004a. Multidrug resistance protein 1-mediated transport of saquinavir by microglia. Neuroreport 15:1183-1186.
43. Dallas S, Schlichter L, Bendayan R. 2004b. MRP4- and MRP5-mediated efflux of 9-(2-phosphonylmethoxyethyl)adenine (PMEA) by microglia. J Pharmacol Exp Ther 309:1221-1229.
44. Dean M RA, Allikmets R. 2001. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156-1166.
45. Diah SK, Smitherman PK, Townsend AJ, 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.
46. Dietrich CG, Ottenhoff R, de Waart DR, Oude Elferink RP. 2001. Role of MRP2 and GSH in intrahepatic cycling of toxins. Toxicology 167:73-81.
47. Draper MP, Martell RL, Levy SB. 1997. Indomethacin-mediated reversal of multidrug resistance and drug efflux in human and murine cell lines overexpressing MRP, but not P-glycoprotein. Br J Cancer 75:810-815.
48. Evers R, Cnubben NH, Wijnholds J, van Deemter L, van Bladeren PJ, Borst P. 1997. Transport of glutathione prostaglandin A conjugates by the multidrug resistance protein 1. FEBS Lett 419:112-116.
49. Evers R, Kool M, van Deemter L, Janssen H, Calafat J, Oomen LC, Paulusma CC, Oude Elferink RP, Baas F, Schinkel AH, Borst P. 1998. Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Invest 101:1310-1319.
50. Evers R, de Haas M, Sparidans R, Beijnen J, Wielinga PR, Lankelma J, Borst P. 2000. Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br J Cancer 83:375-383.
51. Flens MJ, Zaman GJ, van der Valk P, Izquierdo MA, Schroeijers AB, Scheffer GL, van der Groep P, de Haas M, Meijer CJ, Scheper RJ. 1996. Tissue distribution of the multidrug resistance protein. Am J Pathol 148:1237-1247.
52. Fricker G, Miller DS. 2004. Modulation of drug transporters at the blood-brain barrier. Pharmacology 70:169-176.
53. Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu UH, Schulz B, Martinoia E. 2004. Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15:3393-3405.
54. 4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208:345-352.
55. Gerk PM, Vore M. 2002. Regulation of expression of the multidrug resistance-associated protein 2 (MRP2) and its role in drug disposition. J Pharmacol Exp Ther 302:407-415.
56. Germain DP, Remones V, Perdu J, Jeunemaitre X. 2000. Identification of two polymorphisms (c189G>C; c190T>C) in exon 2 of the human MRP6 gene (ABCC6) by screening of Pseudoxanthoma elasticum patients: possible sequence correction? Hum Mutat 16:449.
57. Gheduzzi D, Guidetti R, Anzivino C, Tarugi P, Di Leo E, Quaglino D, Ronchetti IP. 2004. ABCC6 mutations in Italian families affected by pseudoxanthoma elasticum (PXE). Hum Mutat 24:438-439.
58. Gollapudi S, Kim CH, Tran BN, Sangha S, Gupta S. 1997. Probenecid reverses multidrug resistance in multidrug resistance-associated protein-overexpressing HL60/AR and H69/AR cells but not in P-glycoprotein- overexpressing HL60/Tax and P388/ADR cells. Cancer Chemother Pharmacol 40:150-158.
59. Grzywacz MJ, Yang JM, Hait WN. 2003. Effect of the multidrug resistance protein on the transport of the antiandrogen flutamide. Cancer Res 63:2492-2498.
60. Guo Y, Kotova E, Chen ZS, Lee K, Hopper-Borge E, Belinsky MG, Kruh GD. 2003. MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2',3'-dideoxycytidine and 9'-(2'-phosphonylmethoxyethyl)adenine. J Biol Chem 278:29509-29514.
61. Hendrikse NH, Fransseri EJ, van der Graaf WT, Vaalburg W, de Vries EG. 1999. Visualization of multidrug resistance in vivo. Eur J Nucl Med 26:283-293.
62. Hendrikse NH, Kuipers F, Meijer C, Havinga R, Bijleveld CM, van der Graaf WT, Vaalburg W, de Vries EG. 2004. In vivo imaging of hepatobiliary transport function mediated by multidrug resistance associated protein and P-glycoprotein. Cancer Chemother Pharmacol 54:131-138.
63. Higgins C. 1992. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67-113.
64. Hirohashi T SH, Takikawa H, Sugiyama Y. 2000. ATP-dependent transport of bile salts by rat multidrug resistance-associated protein 3 (Mrp3). J Biol Chem 275:2905-2910.
65. Hirohashi T, Suzuki H, Sugiyama Y. 1999. Characterization of the transport properties of cloned rat multidrug resistance-associated protein 3 (MRP3). J Biol Chem 274:15181-15185.
66. Hirouchi M, Suzuki H, Itoda M, Ozawa S, Sawada J, Ieiri I, Ohtsubo K, Sugiyama Y. 2004. Characterization of the cellular localization, expression level, and function of SNP variants of MRP2/ABCC2. Pharm Res 21:742-748.
67. Hooijberg JH, Broxterman HJ, Heijn M, Fies DL, Lankelma J, Pinedo HM. 1997. Modulation by (iso)flavonoids of the ATPase activity of the multidrug resistance protein. FEBS Lett 413:344-348.
68. Hooijberg JH, Broxterman HJ, Kool M, Assaraf YG, Peters GJ, Noordhuis P, Scheper RJ, Borst P, Pinedo HM, Jansen G. 1999a. Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 59:2532-2535.
69. Hooijberg JH, Broxterman HJ, Scheffer GL, Vrasdonk C, Heijn M, de Jong MC, Scheper RJ, Lankelma J, Pinedo HM. 1999b. Potent interaction of flavopiridol with MRP1. Br J Cancer 81:269-276.
70. Hopper E, Belinsky MG, Zeng H, Tosolini A, Testa JR, Kruh GD. 2001. Analysis of the structure and expression pattern of MRP7 (ABCC10), a new member of the MRP subfamily. Cancer Lett 162:181-191.
71. Hopper-Borge E, Chen ZS, Shchaveleva I, Belinsky MG, Kruh GD. 2004. Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 64:4927-4930.
72. Hu X, Peek R, Plomp A, ten Brink J, Scheffer G, van Soest S, Leys A, de Jong PT, Bergen AA. 2003a. Analysis of the frequent R1141X mutation in the ABCC6 gene in pseudoxanthoma elasticum. Invest Ophthalmol Vis Sci 44:1824-1829.
73. Hu X, Plomp AS, van Soest S, Wijnholds J, de Jong PT, Bergen AA. 2003b. Pseudoxanthoma elasticum: a clinical, histopathological, and molecular update. Surv Ophthalmol 48:424-438.
74. Huisman MT, Smit JW, Crommentuyn KM, Zelcer N, Wiltshire HR, Beijnen JH, Schinkel AH. 2002. Multidrug resistance protein 2 (MRP2) transports HIV protease inhibitors, and transport can be enhanced by other drugs. Aids 16:2295-2301.
75. Ilias A UZ, Seidl TL, Le Saux O, Sinko E, Boyd CD, Sarkadi B, Varadi A. 2002. Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 277:16860-16867.
76. Ishikawa T. 1992. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem Sci 17:463-468.
77. Ito K, Suzuki H, Hirohashi T, Kume K, Shimizu T, Sugiyama Y. 1997. Molecular cloning of canalicular multispecific organic anion transporter defective in EHBR. Am J Physiol 272:G16-G22.
78. Ito K, Oleschuk CJ, Westlake C, Vasa MZ, Deeley RG, Cole SP. 2001a. Mutation of Trp1254 in the multispecific organic anion transporter, multidrug resistance protein 2 (MRP2) (ABCC2), alters substrate specificity and results in loss of methotrexate transport activity. J Biol Chem 276:38108-38114.
79. Ito S, Ieiri I, Tanabe M, Suzuki A, Higuchi S, Otsubo K. 2001b. Polymorphism of the ABC transporter genes, MDR1, MRP1 and MRP2/cMOAT, in healthy Japanese subjects. Pharmacogenetics 11:175-184.
80. Jedlitschky G, Leier I, Buchholz U, Barnouin K, Kurz G, Keppler D. 1996. Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res 56:988-994.
81. Jones PM, George AM. 2004. The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 61:682-699.
82. Jorajuria S, Dereuddre-Bosquet N, Becher F, Martin S, Porcheray F, Garrigues A, Mabondzo A, Benech H, Grassi J, Orlowski S, Dormont D, Clayette P. 2004. ATP binding cassette multidrug transporters limit the anti-HIV activity of zidovudine and indinavir in infected human macrophages. Antivir Ther 9:519-528.
83. Kartenbeck J, Leuschner U, Mayer R, Keppler D. 1996. Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome. Hepatology 23:1061-1066.
84. Kawabe T CZ, Wada M, Uchiumi T, Ono M, Akiyama S, Kuwano M. 1999. Enhanced transport of anticancer agents and leukotriene C4 by the human canalicular multispecific organic anion transporter (cMOAT/MRP2). FEBS Lett 456:327-331.
85. Keppler D, Kartenbeck J. 1996. The canalicular conjugate export pump encoded by the cmrp/cmoat gene. Prog Liver Dis 14:55-67.
86. Keppler D, Leier I, Jedlitschky G. 1997. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol Chem 378:787-791.
87. Kiuchi Y SH, Hirohashi T, Tyson CA, Sugiyama Y. 1998. cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett 433:149-152.
88. Klein I, Sarkadi B, Varadi A. 1999. An inventory of the human ABC proteins. Biochim Biophys Acta 1461:237-262.
89. Kobayashi N, Tani T, Hisaka A, Hara K, Yasumori T. 2003. Hepatobiliary transport of a nonpeptidic endothelin antagonist, (+)-(5S,6R,7R)-2-butyl-7- [2((2S)-2-carboxypropyl)4-methoxyphenyl]-5-(3,4- methylenedioxyphenyl) cyclopentenol[1,2-b]pyridine-6-carboxylic acid: uptake by isolated rat hepatocytes and canalicular membrane vesicles. Pharm Res 20:89-95.
90. Koike K, Kawabe T, Tanaka T, Toh S, Uchiumi T, Wada M, Akiyama S, Ono M, Kuwano M. 1997. A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res 57:5475-5479.
91. Konno T, Ebihara T, Hisaeda K, Uchiumi T, Nakamura T, Shirakusa T, Kuwano M, Wada M. 2003. Identification of domains participating in the substrate specificity and subcellular localization of the multidrug resistance proteins MRP1 and MRP2. J Biol Chem 278:22908-22917.
92. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJ, Juijn JA, Baas F, Borst P. 1997. 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 57:3537-3547.
93. Kool M, van der Linden M, de Haas M, Baas F, Borst P 1999a. Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 59:175-182.
94. Kool M, van der Linden M, de Haas M, Scheffer GL, de Vree JM, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, Elferink RP, Baas F, Borst P. 1999b. MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 96:6914-6919.
95. Kruh GD, Belinsky MG. 2003. The MRP family of drug efflux pumps. Oncogene 22:7537-7552.
96. Kullak-Ublick GA, Stieger B, Meier PJ. 2004. Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 126:322-342.
97. Lai L, Tan TM. 2002. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem J 361:497-503.
98. Lang T, Hitzl M, Burk O, Mornhinweg E, Keil A, Kerb R, Klein K, Zanger UM, Eichelbaum M, Fromm MF. 2004. Genetic polymorphisms in the multidrug resistance-associated protein 3 (ABCC3, MRP3) gene and relationship to its mRNA and protein expression in human liver. Pharmacogenetics 14:155-164.
99. Lautier D, Canitrot Y, Deeley RG, Cole SP. 1996. Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem Pharmacol 52:967-977.
100. Le Saux D UZ, Tschuch C, Csiszar K, Bacchelli B, Quaglino D, Pasquali-Ronchetti I, Pope FM, Richards A, Terry S, Bercovitch L, de Paepe A, Boyd CD. 2000. Mutations in a gene encoding an ABC transporter cause pseudoxanthoma elasticum. Nat Genet 25:223-227.
101. Lee K, Klein-Szanto AJ, Kruh GD. 2000. Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells. J Natl Cancer Inst 92:1934-1940.
102. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, Mercer KE, Zhuang Y, Panetta JC, Johnston B, Scheper RJ, Stewart CF, Schuetz JD. 2004. Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24:7612-7621.
103. Leier I, Jedlitschky G, Buchholz U, Cole SP, Deeley RG, Keppler D. 1994. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 269:27807-27810.
104. Leier I, Jedlitschky G, Buchholz U, Center M, Cole SP, Deeley RG, Keppler D. 1996. ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem J 314 (Pt 2):433-437.
105. Leslie EM, Deeley RG, Cole SP. 2001a. Toxicological relevance of the multidrug resistance protein 1, MRP1 (ABCC1) and related transporters. Toxicology 167:3-23.
106. Leslie EM, Ito K, Upadhyaya P, Hecht SS, Deeley RG, Cole SP. 2001b. Transport of the beta-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.
107. Leslie EM, Deeley RG, Cole SP. 2003a. Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab Dispos 31:11-15.
108. Leslie EM, Letourneau IJ, Deeley RG, Cole SP. 2003b. Functional and structural consequences of cysteine substitutions in the NH2 proximal region of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochemistry 42:5214-5224.
109. Leslie EM, Haimeur A, Waalkes MP. 2004. Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J Biol Chem 279:32700-32708.
110. Locher KP. 2004. Structure and mechanism of ABC transporters. Curr Opin Struct Biol 14:426-431.
111. Loe DW, Almquist KC, Cole SP, Deeley RG. 1996. ATP-dependent 17 beta-estradiol 17-(beta-D-glucuronide) transport by multidrug resistance protein (MRP). Inhibition by cholestatic steroids. J Biol Chem 271:9683-9689.
112. Loe DW, Stewart RK, Massey TE, Deeley RG, Cole SP. 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.
113. Loe DW, Deeley RG, Cole SP. 1998. Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58:5130-5136.
114. Lorico A, Nesland J, Emilsen E, Fodstad O, Rappa G. 2002. Role of the multidrug resistance protein 1 gene in the carcinogenicity of aflatoxin B1: investigations using mrp1-null mice. Toxicology 171:201-205.
115. Lorusso V, Pascolo L, Fernetti C, Visigalli M, Anelli P, Tiribelli C. 2002. In vitro and in vivo hepatic transport of the magnetic resonance imaging contrast agent B22956/1: role of MRP proteins. Biochem Biophys Res Commun 293:100-105.
116. Machida I, Inagaki Y, Suzuki S, Hayashi H, Wakusawa S. 2004. Mutation analysis of the multidrug resistance protein 2 (MRP2) gene in a Japanese patient with Dubin-Johnson syndrome. Hepatol Res 30:86-90.
117. Madon J, Hagenbuch B, Landmann L, Meier PJ, Stieger B. 2000. Transport function and hepatocellular localization of mrp6 in rat liver. Mol Pharmacol 57:634-641.
118. Mao Q, Qiu W, Weigl KE, Lander PA, Tabas LB, Shepard RL, Dantzig AH, Deeley RG, Cole SP. 2002. GSH-dependent photolabeling of multidrug resistance protein MRP1 (ABCC1) by [125I]LY475776. Evidence of a major binding site in the COOH-proximal membrane spanning domain. J Biol Chem 277:28690-28699.
119. Marbeuf-Gueye C, Salerno M, Quidu P, Garnier-Suillerot A. 2000. Inhibition of the P-glycoprotein- and multidrug resistance protein-mediated efflux of anthracyclines and calceinacetoxymethyl ester by PAK-104P. Eur J Pharmacol 391:207-216.
120. Masuda M, Ii Y, Yamazaki M, Nishigaki R, Kato Y, Ni'inuma K, Suzuki H, Sugiyama Y. 1997. Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats. Cancer Res 57:3506-3510.
121. McAleer MA, Breen MA, White NL, Matthews N. 1999. pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J Biol Chem 274:23541-23548.
122. Meaden ER, Hoggard PG, Newton P, Tjia JF, Aldam D, Cornforth D, Lloyd J, Williams I, Back DJ, Khoo SH. 2002. P-glycoprotein and MRP1 expression and reduced ritonavir and saquinavir accumulation in HIV-infected individuals. J Antimicrob Chemother 50:583-588.
123. Meloni I, Rubegni P, De Aloe G, Bruttini M, Pianigiani E, Cusano R, Seri M, Mondillo S, Federico A, Bardelli AM, Andreassi L, Fimiani M, Renieri A. 2001. Pseudoxanthoma elasticum: Point mutations in the ABCC6 gene and a large deletion including also ABCC1 and MYH11. Hum Mutat 18:85.
124. Mor-Cohen R, Zivelin A, Rosenberg N, Shani M, Muallem S, Seligsohn U. 2001. Identification and functional analysis of two novel mutations in the multidrug resistance protein 2 gene in Israeli patients with Dubin-Johnson syndrome. J Biol Chem 276:36923-36930.
125. Morrow CS, Diah S, Smitherman PK, Schneider E, Townsend AJ. 1998a. 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.
126. Morrow CS, Smitherman PK, Diah SK, Schneider E, Townsend AJ. 1998b. 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 273:20114-20120.
127. Muller M, Meijer C, Zaman CJR, Borst P, Scheper RJ, Mulder NH, de Vries EGE, Jansen PLM. 1994. Overexpression of the gene encoding the Multidrug resistance-associated protein results in increased ATP dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 91:8822-8826.
128. Naito S, Koike K, Ono M, Machida T, Tasaka S, Kiue A, Koga H, Kumazawa J. 1998. Development of novel reversal agents, imidazothiazole derivatives, targeting MDR1- and MRP-mediated multidrug resistance. Oncol Res 10:123-132.
129. Nakano R, Oka M, Nakamura T, Fukuda M, Kawabata S, Terashi K, Tsukamoto K, Noguchi Y, Soda H, Kohno S. 1998. A leukotriene receptor antagonist, ONO-1078, modulates drug sensitivity and leukotriene C4 efflux in lung cancer cells expressing multidrug resistance protein. Biochem Biophys Res Commun 251:307-312.
130. Nguyen H, Zhang S, Morris ME. 2003. Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J Pharm Sci 92:250-257.
131. Nies AT, Jedlitschky G, Konig J, Herold-Mende C, Steiner HH, Schmitt HP, Keppler D. 2004. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129:349-360.
132. Niewiarowski W, Gendaszewska E, Rebowski G, Wojcik M, Mikolajczyk B, Goss W, Soszynski M, Bartosz G. 2000. Multidrug resistance-associated protein: reduction of expression in human leukaemia cells by antisense phosphorothioate olignucleotides. Acta Biochim Pol 47:1183-1188.
133. Norman BH, Dantzig AH, Kroin JS, Law KL, Tabas LB, Shepard RL, Palkowitz AD, Hauser KL, Winter MA, Sluka JP, Starling JJ. 1999. Reversal of resistance in multidrug resistance protein (MRP1)-overexpressing cells by LY329146. Bioorg Med Chem Lett 9:3381-3386.
134. Nunoya K, Grunt CE, Zhang D, Cole SP, Deeley RG. 2003. Molecular cloning and pharmacological characterization of rat multidrug resistance protein 1 (mrp1). Drug Metab Dispos 31:1016-1026.
135. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, Oude Elferink RP. 1996. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271:1126-1128.
136. Paulusma CC, van Geer MA, Evers R, Heijn M, Ottenhoff R, Borst P, Oude Elferink RP. 1999. Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione. Biochem J 338 (Pt 2):393-401.
137. Paumi CM, Ledford BG, Smitherman PK, Townsend AJ, 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.
138. Payen L, Delugin L, Courtois A, Trinquart Y, Guillouzo A, Fardel O. 1999. Reversal of MRP-mediated multidrug resistance in human lung cancer cells by the antiprogestatin drug RU486. Biochem Biophys Res Commun 258:513-518.
139. Payen L, Delugin L, Courtois A, Trinquart Y, Guillouzo A, Fardel O. 2001. The sulphonylurea glibenclamide inhibits multidrug resistance protein (MRP1) activity in human lung cancer cells. Br J Pharmacol 132:778-784.
140. Peaston AE, Gardaneh M, Franco AV, Hocker JE, Murphy KM, Farnsworth ML, Catchpoole DR, Haber M, Norris MD, Lock RB, Marshall GM. 2001. MRP1 gene expression level regulates the death and differentiation response of neuroblastoma cells. Br J Cancer 85:1564-1571.
141. Pulkkinen L, Nakano A, Ringpfeil F, Uitto J. 2001. Identification of ABCC6 pseudogenes on human chromosome 16p: implications for mutation detection in pseudoxanthoma elasticum. Hum Genet 109:356-365.
142. Qian YM, Song WC, Cui H, Cole SP, Deeley RG. 2001. Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276:6404-6411.
143. Qian YM, Grant CE, Westlake CJ, Zhang DW, Lander PA, Shepard RL, Dantzig AH, Cole SP, Deeley RG. 2002. Photolabeling of human and murine multidrug resistance protein 1 with the high affinity inhibitor [125I]LY475776 and azidophenacyl-[35S]glutathione. J Biol Chem 277:35225-35231.
144. Rappa G, Lorico A, Flavell RA, 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.
145. Rebbeor JF, Connolly GC, Henson JH, Boyer JL, Ballatori N. 2000. ATP-dependent GSH and glutathione S-conjugate transport in skate liver: role of an Mrp functional homologue. Am J Physiol Gastrointest Liver Physiol 279:G417-425.
146. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, Borst P. 2003a. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63:1094-1103.
147. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J, Borst P. 2003b. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Natl Acad Sci USA 100:9244-9249.
148. Rigato I, Pascolo L, Fernetti C, Ostrow JD, Tiribelli C. 2004. The human multidrug-resistance-associated protein MRP1 mediates ATP-dependent transport of unconjugated bilirubin. Biochem J 383:335-341.
149. Ringpfeil F LM, Christiano AM, Uitto J. 2000. Pseudoxanthoma elasticum: mutations in the MRP6 gene encoding a transmembrane ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 97:6001-6006.
150. Rius M, Nies AT, Hummel-Eisenbeiss J, Jedlitschky G, Keppler D. 2003. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38:374-384.
151. Robbiani DF, Finch RA, Jager D, Muller WA, Sartorelli AC, Randolph GJ. 2000. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103:757-768.
152. Ros JE, Libbrecht L, Geuken M, Jansen PL, Roskams TA. 2003. High expression of MDR1, MRP1, and MRP3 in the hepatic-progenitor cell compartment and hepatocytes in severe human liver disease. J Pathol 200:553-560.
153. Salerno M, Garnier-Suillerot A. 2001. Kinetics of glutathione and daunorubicin efflux from multidrug resistance protein overexpressing small-cell lung cancer cells. Eur J Pharmacol 421:1-9.
154. Sampath J, Adachi M, Hatse S, Naesens L, Balzarini J, Flatley RM, Matherly LH, Schuetz JD. 2002. Role of MRP4 and MRP5 in biology and chemotherapy. AAPS Pharm Sci 4:E14.
155. Sasaki M, Suzuki H, Ito K, Abe T, Sugiyama Y. 2002. Transcellular transport of organic anions across a double-transfected Madin-Darby canine kidney II cell monolayer expressing both human organic anion-transporting polypeptide (OATP2/SLC21A6) and Multidrug resistance-associated protein 2 (MRP2/ABCC2). J Biol Chem 277:6497-6503.
156. Scheffer GL, Hu X, Pijnenborg AC, Wijnholds J, Bergen AA, Scheper RJ. 2002. MRP6 (ABCC6) detection in normal human tissues and tumors. Lab Invest 82:515-518.
157. Schuetz EG, Strom S, Yasuda K, Lecureur V, Assem M, Brimer C, Lamba J, Kim RB, Ramachandran V, Komoroski BJ, Venkataramanan R, Cai H, Sinal CJ, Gonzalez FJ, Schuetz JD. 2001. Disrupted bile acid homeostasis reveals an unexpected interaction among nuclear hormone receptors, transporters, and cytochrome P450. J Biol Chem 276:39411-39418.
158. Sinko E, Ilias A, Ujhelly O, Homolya L, Scheffer GL, Bergen AA, Sarkadi B, Varadi A. 2003. Subcellular localization and N-glycosylation of human ABCC6, expressed in MDCKII cells. Biochem Biophys Res Commun 308:263-269.
159. Srivastava SK, Watkins SC, Schuetz E, Singh SV. 2002. Role of glutathione conjugate efflux in cellular protection against benzo[a]pyrene-7,8-diol-9,10- epoxide-induced DNA damage. Mol Carcinog 33:156-162.
160. Stewart AJ, Canitrot Y, Baracchini E, Dean NM, Deeley RG, Cole SP. 1996. Reduction of expression of the multidrug resistance protein (MRP) in human tumor cells by antisense phosphorothioate oligonucleotides. Biochem Pharmacol 51:461-469.
161. Stride BD, Valdimarsson G, Gerlach JH, Wilson GM, Cole SP, Deeley RG. 1996. Structure and expression of the messenger RNA encoding the murine multidrug resistance protein, an ATP-binding cassette transporter. Mol Pharmacol 49:962-971.
162. Suzuki H, Sugiyama Y. 2002. Single nucleotide polymorphisms in multidrug resistance associated protein 2 (MRP2/ABCC2): its impact on drug disposition. Adv Drug Deliv Rev 54:1311-1331.
163. Tammur J PC, Arnould I, Rzhetsky A, Hutchinson A, Adachi M, Schuetz JD, Swoboda KJ, Ptacek LJ, Rosier M, Dean M, Allikmets R. 2001. Two new genes from the human ATP-binding cassette transporter superfamily, ABCC11 and ABCC12, tandemly duplicated on chromosome 16q12. Gene 2001;273:89-96.
164. Terlouw SA, Graeff C, Smeets PH, Fricker G, Russel FG, Masereeuw R, Miller DS. 2002. Short- and long-term influences of heavy metals on anionic drug efflux from renal proximal tubule. J Pharmacol Exp Ther 301:578-585.
165. Toh S, Wada M, Uchiumi T, Inokuchi A, Makino Y, Horie Y, Adachi Y, Sakisaka S, Kuwano M. 1999. Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/ cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome. Am J Human Genet 64:739-746.
166. Uitto J. 2004. Pseudoxanthoma elasticum-a connective tissue disease or a metabolic disorder at the genome/environment interface? J Invest Dermatol 122:ix-x.
167. van Aubel A, Smeets PH, Peters JG, Bindels RJ, Russel FG. 2002a. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 13:595-603.
168. van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG. 2002b. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 13:595-603.
169. van Aubel RA, Smeets PH, Van Den Heuvel JJ, Russel FG. 2004. Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites. Am J Physiol Renal Physiol.
170. Versantvoort CH, Broxterman HJ, Lankelma J, Feller N, Pinedo HM. 1994. Competitive inhibition by genistein and ATP dependence of daunorubicin transport in intact MRP overexpressing human small cell lung cancer cells. Biochem Pharmacol 48:1129-1136.
171. Versantvoort CH, Broxterman HJ, Bagrij T, Scheper RJ, Twentyman PR. 1995. Regulation by glutathione of drug transport in multidrug-resistant human lung tumour cell lines overexpressing multidrug resistance-associated protein. Br J Cancer 72:82-89.
172. Wakusawa S, Machida I, Suzuki S, Hayashi H, Yano M, Yoshioka K. 2003. Identification of a novel 2026G ->C mutation of the MRP2 gene in a Japanese patient with Dubin-Johnson syndrome. J Hum Genet 48:425-429.
173. Wall M, Wani MC, Cook CE, Palmer KH, Mcphail AT, Sim GA. 1966. Plant antitumor agents: 1, the isolation and structure of camptothecin, anovel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminata. J Am Chem Soc 88:3888-3890.
174. Wielinga PR, Reid G, Challa EE, van der Heijden I, van Deemter L, de Haas M, Mol C, Kuil AJ, Groeneveld E, Schuetz JD, Brouwer C, De Abreu RA, Wijnholds J, Beijnen JH, Borst P. 2002. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharmacol 62:1321-1331.
175. Wielinga PR, van der Heijden I, Reid G, Beijnen JH, Wijnholds J, Borst P. 2003. Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J Biol Chem 278:17664-17671.
176. Wijnholds J, Evers R, van Leusden MR, Mol CA, Zaman GJ, Mayer U, Beijnen JH, van der Valk M, Krimpenfort P, Borst P. 1997. Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3:1275-1279.
177. Wijnholds J, Scheffer GL, van der Valk M, van der Valk P, Beijnen JH, Scheper RJ, Borst P. 1998. Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med 188:797-808.
178. Wijnholds J, Mol CA, van Deemter L, de Haas M, Scheffer GL, Baas F, Beijnen JH, Scheper RJ, Hatse S, De Clercq E, Balzarini J, Borst P. 2000. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc Natl Acad Sci USA 97:7476-7481.
179. Williams GC, Liu A, Knipp G, Sinko PJ. 2002. Direct evidence that saquinavir is transported by multidrug resistance-associated protein (MRP1) and canalicular multispecific organic anion transporter (MRP2). Antimicrob Agents Chemother 46:3456-3462.
180. Xiong H, Turner KC, Ward ES, Jansen PL, Brouwer KL. 2000. Altered hepatobiliary disposition of acetaminophen glucuronide in isolated perfused livers from multidrug resistance-associated protein 2-deficient TR(-) rats. J Pharmacol Exp Ther 295:512-518.
181. Xiong H, Suzuki H, Sugiyama Y, Meier PJ, Pollack GM, Brouwer KL. 2002. Mechanisms of impaired biliary excretion of acetaminophen glucuronide after acute phenobarbital treatment or phenobarbital pretreatment. Drug Metab Dispos 30:962-969.
182. Yabuuchi H SH, Takayanagi S, Ishikawa T. 2001. Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem Biophys Res Commun 288:933-939.
183. Yang Z, Horn M, Wang J, Shen DD, Ho RJ. 2004. Development and characterization of a recombinant Madin-Darby canine kidney cell line that expresses rat multidrug resistance-associated protein 1 (rMRP1). AAPS PharmSci 6:E8.
184. Zaman GJ, Versantvoort CH, Smit JJ, Eijdems EW, de Haas M, Smith AJ, Broxterman HJ, Mulder NH, de Vries EG, Baas F. 1993. Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res 53:1747-1750.
185. Zaman GJ, 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.
186. Zaman GJ, Lankelma J, van Tellingen O, Beijnen J, Dekker H, Paulusma C, Oude Elferink RP, Baas F, Borst P. 1995. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc Natl Acad Sci USA 92:7690-7694.
187. Zaman GJ, Cnubben NH, van Bladeren PJ, Evers R, Borst P. 1996. Transport of the glutathione conjugate of ethacrynic acid by the human multidrug resistance protein MRP. FEBS Lett 391:126-130.
188. Zelcer N, Saeki T, Reid G, Beijnen JH, Borst P. 2001. Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 276:46400-46407.
189. Zelcer N, Huisman MT, Reid G, Wielinga P, Breedveld P, Kuil A, Knipscheer P, Schellens JH, Schinkel AH, Borst P. 2003a. Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). J Biol Chem 278:23538-23544.
190. Zelcer N, Reid G, Wielinga P, Kuil A, van der Heijden I, Schuetz JD, Borst P. 2003b. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem J 371:361-367.
191. Zeng H, Bain LJ, Belinsky MG, Kruh GD. 1999. Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents. Cancer Res 59:5964-5967.
192. Zeng H, Liu G, Rea PA, Kruh GD. 2000. Transport of amphipathic anions by human multidrug resistance protein 3. Cancer Res 60:4779-4784.
193. Zeng H, Chen ZS, Belinsky MG, Rea PA, Kruh GD. 2001. Transport of methotrexate (MTX) and folates by multidrug resistance protein (MRP) 3 and MRP1: effect of polyglutamylation on MTX transport. Cancer Res 61:7225-7232.
194. Zhang DW, Cole SP, Deeley RG. 2001. Identification of a nonconserved amino acid residue in multidrug resistance protein 1 important for determining substrate specificity: evidence for functional interaction between transmembrane helices 14 and 17. J Biol Chem 276:34966-34974.
195. Zhang DW, Nunoya K, Vasa M, Gu HM, Theis A, Cole SP, Deeley RG. 2004. Transmembrane helix 11 of multidrug resistance protein 1 (MRP1/ABCC1): identification of polar amino acids important for substrate specificity and binding of ATP at nucleotide binding domain 1. Biochemistry 43:9413-9425.
196. Zhao Q, Chang XB. 2004. Mutation of the aromatic amino acid interacting with adenine moiety of ATP to a polar residue alters the properties of multidrug resistance protein 1. J Biol Chem 279:48505-48512.
197. Zimmermann C, Gutmann H, Hruz P, Gutzwiller JP, Beglinger C, Drewe J. 2005. Mapping of MDR1 and MRP1-5 mRNA expression along the human intestinal tract. Drug Metab Dispos 33:219-224.
198. Zollner G, Fickert P, Silbert D, Fuchsbichler A, Marschall HU, Zatloukal K, Denk H, Trauner M. 2003. Adaptive changes in hepatobiliary transporter expression in primary biliary cirrhosis. J Hepatol 38:717-727.