Biology of the multidrug resistance-associated protein, MRP

European Journal of Cancer

Volumn 32, Issue 6, 1996, Pages 945-957

  Loe, D W ^a   Deeley, R G ^a   Cole, S P C ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; CEPHARANTHINE; DINITROPHENYLHAPTEN; DOXORUBICIN; EPIRUBICIN; ESTRADIOL 17 GLUCURONIDE; ETOPOSIDE; GELDANAMYCIN; GENE PRODUCT; GLUTATHIONE; GLUTATHIONE DERIVATIVE; GLUTATHIONE DISULFIDE; GLYCOPROTEIN P; LEUKOTRIENE C4; MEZEREIN; NOVOBIOCIN; VINCRISTINE;

ANIMAL CELL; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; COLON CARCINOMA; DRUG TRANSPORT; ERYTHROLEUKEMIA; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW;

DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM PROTEINS; NEOPLASMS; P-GLYCOPROTEIN;

EID: 0029954845     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/0959-8049(96)00046-9     Document Type: Article

References (188)

1. Cole SPC. Multidrug resistance in human lung cancer and topoisomerase II. In Pass HI, Mitchell J, Johnson DH, Turrisi AT, eds. Lung Cancer: Principles and Practice. Philadelphia, JB Lippincott, 1996, 169-204.
2. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993, 62, 385-427.
3. Georges E, Sharom FJ, Ling V. Multidrug resistance and chemosensitization: therapeutic implications for cancer chemotherapy. Adv Pharmacol 1990, 21, 185-220.
4. Cole SPC. The 1991 Merck Frosst award. Multidrug resistance in small cell lung cancer. Can J Physiol Pharmacol 1992, 70, 313-329.
5. Endicott JA, Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 1989, 58, 137-171.
6. Cole SPC. Drug resistance and lung cancer. In Wood J, ed. Cancer: Concept to Clinic. Fairlawn NJ, Medical Publishing Enterprises, 1992, 15-21.
7. Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full-length cDNA for the human MDR1 gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci USA 1987, 84, 3004-3008.
8. Gros P, Neriah YB, Croop JM, Housman DE. Isolation and expression of a complementary DNA that confers multidrug resistance. Nature 1986, 323, 728-731.
9. Riordan JR, Deuchars K, Kartner N, Alon N, Trent J, Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985, 316, 817-819.
10. Lincke CR, Van der Blick AM, Schuurhuis GJ, Van der Velde-Koerts T, Smit JJM, Borst P. Multidrug resistance phenotype of human BRO melanoma cells transfected with a wild-type human mdr1 complementary DNA. Cancer Res 1990, 50, 1779-1785.
11. Cole SPC, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258, 1650-1654.
12. Cole SPC, Deeley RG. Multidrug resistance-associated protein: sequence correction. Science 1993, 260, 879.
13. Grant CE, Valdimarsson G, Hipfner DR, Almquist KC, Cole SPC, Deeley RG. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res 1994, 54, 357-361.
14. Zaman GJR, Flens MJ, van Leusden MR, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 1994, 91, 8822-8826.
15. Kruh GD, Chan A, Myers K, Gaughan K, Miki T, Aaronson SA. Expression complementary DNA library transfer establishes mrp as a multidrug resistance gene. Cancer Res 1994, 54, 1649-1652.
16. Cole SPC, Deeley RG. Multidrug resistance associated with overexpression of MRP. In Hait WN, ed. Advances in Cancer Research. Kluwer Academic, 1996, in press.
17. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992, 8, 67-113.
18. Ames GFL. Bacterial periplasmic permeases as model systems for the superfamily of traffic ATPases, including the multidrug resistance protein and the cystic fibrosis transmembrane conductance regulator. Int Rev Cytol 1992, 137A, 1-35.
19. Cole SPC, Sparks KE, Fraser K, et al. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 1994, 54, 5902-5910.
20. Muller M, Meijer C, Zaman GJR, et al. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 1994, 91, 13033-13037.
21. Brock I, Hipfner DR, Nielsen BS, et al. Sequential coexpression of the multidrug resistance genes MRP and mdr1 and their products in VP-16 (etoposide)-selected H69 small cell lung cancer cells. Cancer Res 1995, 55, 459-462.
22. Slapak CA, Mizunuma N, Kufe DW. Expression of the multidrug resistance associated protein and P-glycoprotein in doxorubicin-selected human myeloid leukemia cells. Blood 1994, 84, 3113-3121.
23. Hasegawa S, Abe T, Naito S, et al. Expression of multidrug resistance-associated protein (MRP), MDR1, and DNA Topoisomerase II in human multidrug-resistant bladder cancer cell lines. Br J Cancer 1995, 71, 907-913.
24. Nielsen D, Skovsgaard T. P-glycoprotein as multidrug transporter: a critical review of current multidrug resistant cell lines. Biochem Biophys Acta 1992, 1139, 169-183.
25. Nooter K, Herweijer H. Multidrug resistance (mdr) genes in human cancer. Br J Cancer 1991, 63, 663-669.
26. Pastan I, Gottesman MM. Multidrug resistance. Annu Rev Med 1991, 42, 277-286.
27. Mirski SEL, Gerlach JH, Cole SPC. Multidrug resistance in a human small cell lung cancer cell line selected in adriamycin. Cancer Res 1987, 47, 2594-2598.
28. Cole SPC, Chanda ER, Dicke FP, Gerlach JH, Mirski SEL. Non-P-glycoprotein-mediated multidrug resistance in a small cell lung cancer cell line: evidence for decreased susceptibility to drug-induced DNA damage and reduced levels of topoisomerase II. Cancer Res 1991, 51, 3345-3352.
29. Evans CD, Mirski SEL, Danks MK, Cole SPC. Reduced levels of topoisomerase II α and β in a multidrug resistant small cell lung cancer cell line. Cancer Chemother Pharmacol 1994, 34, 242-248.
30. Cole SPC, Pinkoski MJ, Bhardwaj G, Deeley RG. Elevated expression annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line. Br J Cancer 1992, 65, 498-502.
31. Cole SPC, Downes HF, Mirski SEL, Clements DJ. Alterations in glutathione and glutathione-related enzymes in a multidrug-resistant small cell lung cancer cell line. Mol Pharmacol 1990, 37, 192-197.
32. Slovak ML, Ho JP, Bhardwaj G, Kurz EU, Deeley RG, Cole SPC. Localization of a novel multidrug resistance-associated gene in the HT1080/DR4 and H69AR human tumor cell lines. Cancer Res 1993, 53, 3221-3225.
33. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982, 1, 945-951.
34. Higgins CF. Export-import family expands. Nature 1989, 340, 342.
35. Doige CA, Ames GF-L. ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Annu Rev Microbiol 1993, 47, 291-319.
36. Riordan JR, Rommens JM, Kerem B-S, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245, 1066-1073.
37. Welsh MJ, Smith AE. Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 1993, 73, 1251-1254.
38. Kelly A, Powis SH, Kerr L-A, et al. Assembly and function of the two ABC ransporter proteins encoded in the human major histocompatibility complex. Nature 1992, 355, 641-644.
39. Neefjes JJ, Momburg F, Hammerling GJ. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 1993, 261, 769-771.
40. Gerlach JH, Endicott JA, Juranka PF, et al. Homology between P-glycoprotein and a bacterial hemolysin transport protein suggests a model for multidrug resistance. Nature 1986, 324, 485-489.
41. Aguilar-Bryan L, Nichols CG, Wechsler SW, et al. Cloning of the β cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 1995, 268, 423-426.
42. Thomas PM, Cote GJ, Wohlik N, et al. Mutations in the sulfonylurea receptor gene in familial persistent hyperinsulinemic hypoglycemia of infancy. Science 1995, 268, 426-429.
43. Stride BD, Valdimarsson G, Gerlach JH, Cole SPC, Deeley RG. Structure and expression of the mRNA encoding the murine multidrug resistance protein (MRP), an ATP-binding cassette transporter. Mol Pharmacol 1996, in press.
44. - channels in normal and cystic fibrosis airway epithelial cells by extracellular ATP. Proc Natl Acad Sci USA 1992, 89, 1621-1625.
45. Gadsby DC, Nagel G, Hwang T-C. The CFTR chloride channel of mammalian heart. Annu Rev Physiol 1995, 57, 387-416.
46. Papadopoulou B, Roy G, Dey S, Rosen BP, Ouellette M. Contribution of the Leishmania P-glycoprotein-related gene ItpgpA to oxyanion resistance. J Biol Chem 1994, 269, 11980-11986.
47. Callahan HL, Beverley SM. Heavy metal resistance: a new role for P-glycoproteins in Leishmania. J Biol Chem 1991, 266, 18427-18430.
48. Katzmann DJ, Hallstrom TC, Voet M, et al. Expression of an ATP-binding cassette transporter-encoding gene (YORI) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol Cell Biol 1995, 15, 6875-6883.
49. Szczypka MS, Wemmie JA, Moye-Rowley WS, Thiele DJ. A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J Biol Chem 1994, 269, 22853-22857.
50. r 190,000 multidrug resistance protein (MRP) in drug-selected and transfected human tumor cells. Cancer Res 1995, 55, 102-110.
51. Krishnamachary N, Center MS. The MRP gene associated with a non-P-glycoprotein multidrug resistance encodes a 190-kDa membrane bound glycoprotein. Cancer Res 1993, 53, 3658-3661.
52. Ma L, Krishnamachary N, Center MS. Phosphorylation of the multidrug resistance associated protein gene encoded protein P190. Biochemistry 1995, 34, 3338-3343.
53. 4 sub-lines with increasing adriamycin resistance. Int J Cancer 1995, 61, 375-380.
54. Hare JF. Mechanisms of membrane protein turnover. Biochem Biophys Acta 1990, 1031, 71-90.
55. Cohen D, Yang C-PH, Horwitz SB. The products of the mdr1a and mdr1b genes from multidrug resistant murine cells have similar degradation rates. Life Sci 1990, 46, 489-495.
56. Yoshimura A, Kuwazuru Y, Sumizawa T, et al. Biosynthesis, processing and half-life of P-glycoprotein in a human multidrug-resistant KB cells. Biochem Biophys Acta 1989, 992, 307-314.
57. Ward CL, Kopito RR. Intracellular turnover of cystic fibrosis transmembrane conductance regulator - inefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 1994, 269, 25710-25718.
58. Ward CI, Omura S, Kopito RR. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 1995, 83, 121-127.
59. Becq F, Jensen TJ, Chang X-B, et al. Phosphatase inhibitors activate normal and defective CFTR chloride channels. Proc Natl Acad Sci USA 1994, 91, 9160-9164.
60. Picciotto MR, Cohn JA, Bertuzzi G, Greengard P, Nairn AC. Phosphorylation of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 1992, 267, 12742-12752.
61. Chambers TC, Pohl J, Raynor RL, Kui JF. Identification of specific sites in human P-glycoprotein phosphorylated by protein kinase C. J Biol Chem 1993, 268, 4592-4595.
62. Orr GA, Han EK-H, Browne PC, et al. Identification of the major phosphorylation domain of murine mdr1b P-glycoprotein analysis of the protein kinase A and protein kinase C phosphorylation sites. J Biol Chem 1993, 268, 25054-25062.
63. Loe DW, Almquist KC, Hipfner DR, Mackie JE, Cole SPC, Deeley RG. Characterization of the 190 kDa multidrug resistance protein (MRP) in drug-selected and transfected human tumor cells. Proc Am Assoc Cancer Res 1995, 36, 322.
64. Epand RM, Stafford AR. Protein kinases and multidrug resistance. Cancer J 1993, 6, 154-158.
65. Kuss BJ, Deeley RG, Cole SPC, et al. Deletion of gene for multidrug resistance in acute myeloid leukaemia with inversion in chromosome 16: prognostic implications. Lancet 1994, 343, 1531-1534.
66. Eijdems EWHM, De Haas M, Coco-Martin JM, et al. Mechanisms of MRP over-expression in four human lung-cancer cell lines and analysis of the MRP amplicon. Int J Cancer 1995, 60, 676-684.
67. Slapak CA, Fracasso PM, Martell RL, Toppmeyer DL, Lecerf J-M, Levy SB. Overexpression of the multidrug resistance-associated protein (MRP) in vincristine but not doxorubicin-selected multidrug-resistant murine erythroleukemia cells. Cancer Res 1994, 54, 5607-5613.
68. Kurz EU, Grant CE, Vasa MZ, Burtch-Wright RA, Cole SPC, Deeley RG. Analysis of the proximal promoter region of the multidrug resistance protein (MRP) gene in three small cell lung cancer cell lines. Proc Am Assoc Cancer Res 1995, 36, 1917.
69. Zhu Q, Center MS. Cloning and sequence analysis of the promoter region of the MRP gene of HL60 cells isolated for resistance to adriamycin. Cancer Res 1994, 54, 4488-4492.
70. Monckton DG, Caskey CT. Unstable triplet repeat diseases. Circulation 1995, 91, 513-520.
71. Leier I, Jedlitschky G, Buchholz U, Cole SPC, Deeley RG, Keppler D. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 1994, 269, 27807-27810.
72. Jedlitschky G, Leier I, Buchholz U, Center M, Keppler D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res 1994, 54, 4833-4836.
73. 4 and chemotherapeutic agents in membrane vesicles: demonstration of glutathione-dependent vincristine transport. J Biol Chem, in press.
74. Keppler D. Leukotrienes: biosynthesis, transport, inactivation, and analysis. Rev Physiol Biochem Pharmacol 1992, 121, 1-30.
75. 4 synthase. Proc Natl Acad Sci USA 1994, 91, 9745-9749.
76. Hay DWP, Torphy TJ, Undem BJ. Cysteinyl leukotrienes in asthma: old mediators up to new tricks. Trends Pharmacol Sci 1995, 16, 304-309.
77. Mayer R, Kartenbeck J, Buchler M, Jedlitschky G, Leier I, Keppler D. Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport-deficient mutant hepatocytes. J Cell Biol 1995, 131, 137-150.
78. Ishikawa T, Ali-Osman F. Glutathione-associated cisdiamminedichloroplatinum(II) metabolism and ATP-dependent efflux from leukemia cells. J Biol Chem 1993, 268, 20116-20125.
79. Oude Elferink RPJ, Jansen PLM. The role of the canalicular multispecific organic anion transporter in the disposal of endo- and xenobiotics. Pharmacol Ther 1994, 64, 77-97.
80. Akerboom TPM, Narayanaswami V, Kunst M, Sies H. ATP-dependent S-(2,4-dinitrophenyl)glutathione transport in canalicular plasma membrane vesicles from rat liver. J Biol Chem 1991, 226, 13147-13152.
81. Leier I, Jedlitschky G, Buchholz U, Keppler D. Characterization of the ATP-dependent leukotriene C4 export carrier in mastocytoma cells. Eur J Biochem 1994, 220, 599-606.
82. Ishikawa T, Muller M, Klunemann C, Schaub T, Keppler D. ATP-dependent primary active transport of cysteinyl leukotrienes across liver canalicular membranes. J Biol Chem 1990, 265, 19279-19286.
83. 2+-dependent cardiac transport system for glutathione S-conjugates - a study using rat heart sarcolemma vesicles. J Biol Chem 1989, 264, 17343-17348.
84. Scott N, Hatlelid KM, MacKenzie NE, Carter DE. Reactions of arsenic (III) and arsenic(V) species with glutathione. Chem Res Toxicol 1993, 6, 102-106.
85. Delnomdedieu M, Basti MM, Otvos JD, Thomas DJ. Transfer of arsenite from glutathione to dithiols: a model of interaction. Chem Res Toxicol 1993, 6, 598-602.
86. Leier I, Jedlitschky G, Buchholz U, et al. ATP-dependent glutathione disulfide transport mediated by the MRP gene-encoded conjugate export pump. Biochem J 1996, 314, 433-437.
87. Loe DW, Almquist KC, Cole SPC, Deeley RG. ATP-dependent 17β-estradiol 17-(β-D-glucuronide) transport by multidrug resistance protein: inhibition by cholestatic steroids. J Biol Chem, in press.
88. -) rats with conjugated hyperbilirubinemia. Proc Natl Acad Sci USA 1990, 87, 3557-3561.
89. - rat liver canalicular membranes. Am J Physiol 1992, 262, G629-G635.
90. Nishida T, Gatmaitan Z, Roy-Chowdhry J, Arias IM. Two distinct mechanisms for bilirubin glucuronide transport by rat bile canalicular membrane vesicles - demonstration of defective ATP-dependent transport in rats (TR-) with inherited conjugated hyperbilirubinemia. J Clin Invest 1992, 90, 2130-2135.
91. Verkade HJ, Wolbers MJ, Havinga R, Uges DRA, Vonk RJ, Kuipers F. The uncoupling of biliary lipid from bile acid secretion by organic anions in the rat. Gastroenterology 1990, 99, 1485-1492.
92. DeHerder WW, Van der Hul RL, Bonthuis F, Jansen PLM, Oude Elferink RPJ, Visser TJ. Pathways for the biliary excretion of T3 conjugates. Ann Endocrin 1989, 50, 98.
93. Oude Elferink RPJ, Meijer DKF, Kuipers F, Jansen PLM, Groen AK, Groothuis GMM. Hepatobiliary secretion of organic compounds; molecular mechanisms of membrane transport. Biochem Biophys Acta 1995, 1241, 215-268.
94. Roelofsen H, Vos T, van der Deen M, Moshage H, Jansen PLM, Muller M. Localization of the multidrug resistance protein (MRP) and P-glycoprotein (Pgp) in polarized HepG2 cells: comparison with the distribution of transport activity. Hepatology 1995, 22, 312A.
95. Ruetz S, Brault M, Kast C, et al. Functional expression of the multidrug resistance-associated protein (MRP) in the yeast Saccharomyces cerevisiae. J Biol Chem 1996, 271, 4154-4160.
96. Raymond M, Gros P, Whiteway M, Thomas DY. Functional complementation of yeast STE6 by a mammalian multidrug resistance mdr gene. Science 1992, 256, 232-234.
97. Jovov B, Ismailov II, Benos DJ. Cystic fibrosis transmembrane conductance regulator is required for protein kinase A activation of an outwardly rectified anion channel purified from bovine tracheal epithelia. J Biol Chem 1995, 270, 1521-1528.
98. Gabriel SE, Clarke LL, Boucher RC, Stutts MJ. CFTR and outward rectifying chloride channels are distinct proteins with a regulatory relationship. Nature 1993, 363, 263-266.
99. Hardy SP, Goodfellow HR, Valverde MA, Gill DR, Sepulveda FV, Higgins CF. Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO J 1995, 14, 68-75.
100. Higgins CF. Volume-activated chloride currents associated with the mutidrug resistance P-glycoprotein. J Physiol 1995, 482, 31S-36S.
101. KATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 1995, 270, 1166-1170.
102. + channels and volume-regulated anion channels in multidrug-resistant small cell lung cancer cells. Cancer Res 1993, 53, 4156-4160.
103. Jirsch JD, Loe DW, Cole SPC, Deeley RG, Fedida D. ATP is not required for volume-activated anion current in multidrug-resistant small cell lung cancer cells. Am J Physiol 1994, 268, C688-C699.
104. Abbaszadegan MR, Futscher BW, Klimecki WT, List A, Dalton WS. Analysis of multidrug resistance-associated protein (MRP) messenger RNA in normal and malignant hematopoietic cells. Cancer Res 1994, 54, 4676-4679.
105. Zaman GJR, Versantvoort CHM, Smit JJM, et al. 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 1993, 53, 1747-1750.
106. Kruh GD, Gaughan KT, Godwin A, Chan A. Expression pattern of MRP in human tissues and adult solid tumor cell lines. J Natl Cancer Inst 1995, 87, 1256-1258.
107. r 190,000 multidrug resistance protein, MRP, with monoclonal antibodies. Cancer Res 1994, 54, 5788-5792.
108. Flens MJ, Izquierdo MA, Scheffer GL, et al. Immunochemical detection of the multidrug resistance-associated protein MRP in human multidrug-resistant tumor cells by monoclonal antibodies. Cancer Res 1994, 54, 4557-4563.
109. Breuninger LM, Paul S, Gaughan K, et al. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res 1995, 55, 5342-5347.
110. Kirschner LS, Greenberger LM, Hsu SI-H, et al. Biochemical and genetic characterization of the multidrug resistance pheno-type in murine macrophage-like J774.2 cells. Biochem Pharmacol 1992, 43, 77-87.
111. Bech-Hansen NT, Till JE, Ling V. Pleiotropic phenotype of colchicine-resistant CHO cells: cross-resistance and collateral sensitivity. J Cell Physiol 1976, 88, 23-32.
112. Doige CA, Sharom FJ. Transport properties of P-glycoprotein in plasma membrane vesicles from multidrug-resistant Chinese hamster ovary cells. Biochem Biophys Acta 1992, 1109, 161-171.
113. Horio M, Gottesman MM, Pastan I. ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc Natl Acad Sci USA 1988, 85, 3580-3584.
114. Sharom FJ, Yu X, Doige CA. Functional reconstitution of drug transport and ATPase activity in proteoliposomes containing partially purified P-glycoprotein. J Biol Chem 1993, 268, 24197-24202.
115. Shapiro AB, Ling V. Reconstitution of drug transport by purified P-glycoprotein. J Biol Chem 1994, 270, 16167-16175.
116. McGrath T, Center MS. Mechanisms of multidrug resistance in HL60 cells: evidence that a surface membrane protein distinct from P-glycoprotein contributes to reduced cellular accumulation of drug. Cancer Res 1988, 48, 3959-3963.
117. Schuurhuis GJ, van Heijningen THM, Cervantes A, et al. Changes in subcellular doxorubicin distribution and cellular accumulation alone can largely account for doxorubicin resistance in SW-1573 lung cancer and MCF-7 breast cancer multidrug resistant tumour cells. Br J Cancer 1993, 68, 898-908.
118. Barrand MA, Rhodes T, Center MS, Twentyman PR. Chemo-sensitization 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 1993, 29A, 408-415.
119. Binaschi M, Supino R, Gambetta RA, et al. MRP gene over-expression in a human doxorubicin-resistant SCLC cell line: alterations in cellular pharmacokinetics and in pattern of cross-resistance. Int J Cancer 1995, 62, 84-89.
120. Marquardt D, Center MS. Drug transport mechanisms in HL60 cells isolated for resistance to adriamycin: evidence for nuclear drug accumulation and redistribution in resistant cells. Cancer Res 1992, 52, 3157-3163.
121. Coley HM, Amos WB, Twentyman PR, Workman P. Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localization of anthracyclines in parent and multidrug resistant cell lines. Br J Cancer 1993, 67, 1316-1323.
122. Hindenburg AA, Baker MA, Gleyzer E, Stewart VJ, Case N, Taub RN. Effect of verapamil and other agents on the distribution of anthracyclines and on reversal of drug resistance. Cancer Res 1987, 47, 1421-1425.
123. Gervasoni JE, Fields SZ, Krishna S, et al. Subcellular distribution of daunorubicin in P-glycoprotein-positive and -negative drug-resistant cell lines using laser-assisted confocal microscopy. Cancer Res 1991, 51, 4955-4963.
124. Hindenburg AA, Gervasoni JE, Krishna S, et al. Intracellular distribution and pharmacokinetics of daunorubicin in anthracycline-sensitive and -resistant HL-60 cells. Cancer Res 1989, 49, 4607-4614.
125. Schuurhuis GJ, Broxterman HJ, de Lange JHM, et al. Early multidrug resistance, defined by changes in intracellular doxorubicin distribution, independent of P-glycoprotein. Br J Cancer 1991, 64, 857-861.
126. Barrand MA, Robertson KJ, Neo S-Y, et al. Localization of the multidrug resistance-associated protein, MRP, in resistant large-cell lung tumour cells. Biochem Pharmacol 1995, 50, 1725-1729.
127. 2 complex. J Cell Biol 1993, 123, 1119-1132.
128. Burgoyne RD, Clague MJ. Annexins in the endocytic pathway. Trends Biochem Sci 1994, 19, 231-232.
129. Safa AR. Photoaffinity labelling of P-glycoprotein in multidrug-resistant cells. Cancer Invest 1992, 10, 295-305.
130. McGrath T, Latoud C, Arnold ST, Safa AR, Felsted RL, Center Ms. Mechanisms of multidrug resistance in HL60 cells - analysis of resistance associated membrane proteins and levels of mdr gene expression. Biochem Pharmacol 1989, 38, 3611-3619.
131. Tew KD. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res 1994, 54, 4313-4320.
132. Versantvoort CHM, Broxterman HJ, Bagrij T, Scheper RJ, Twentyman PR. Regulation by glutathione of drug transport in multidrug resistant human lung tumour cell lines overexpressing MRP. Br J Cancer 1995, 72, 82-89.
133. Zaman GJR, Lankelma J, Van Tellingen O, et al. Role of glutathione in the export of compounds from cells by the multi-drug-resistance-associated protein. Proc Natl Acad Sci USA 1995, 92, 7690-7694.
134. Ford JM, Hait WN. Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol Rev 1990, 42, 155-199.
135. Ford JM, Hait WN. Pharmacologie circumvention of multidrug resistance. Cytotechnology 1993, 12, 171-212.
136. Safa AR. Photoaffinity labelling of the multidrug-resistance-related P-glycoprotein with photoactive analogs of verapamil. Proc Natl Acad Sci USA 1988, 85, 7187-7191.
137. Sharom FJ, Yu X, Chu JWK, Doige CA. Characterization of the ATPase activity of P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochem J 1995, 308, 381-390.
138. Cole SPC, Downes HF, Slovak ML. Effect of calcium antagon-ists on the chemosensitivity of two multidrug resistant human tumour cell lines which do not overexpress P-glycoprotein. Br J Cancer 1989, 59, 42-46.
139. Gollapudi S, Gupta S. Lack of reversal of daunorubicin resistance in HL60/AR cells by cyclosporin A. Anticancer Res 1992, 12, 2127-2132.
140. Abe T, Koike K, Ohga T, et al. Chemosensitisation of spontaneous multidrug resistance by a 1,4-dihydropyridine analogue and verapamil in human glioma cell lines overexpressing MRP or MDR1. Br J Cancer 1995, 72, 418-423.
141. Slovak ML, Hoeltge GA, Dalton WS, Trent JM. Pharmacological and biological evidence for differing mechanisms of doxorubicin resistance in two human tumor cell lines. Cancer Res 1988, 48, 2793-2797.
142. Davey RA, Longhurst TJ, Davey MW, et al. Drug resistance mechanisms and MRP expression in response to epirubicin treatment in a human leukaemia cell line. Leukemia Res 1995, 17, 1-8.
143. Tasaki Y, Nakagawa M, Ogata J, Kiue A, Tanimura H, Kuwano M, Nomura Y. Reversal by a dihydropyridine derivative of non-P-glycoprotein-mediated multidrug resistance in etoposide-resistant human prostatic cancer cell line. J Urol 1995, 154, 1210-1216.
144. Gekeler V, Boer R, Ise W, Sanders KH, Schachtele C, Beck J. The specific bisindolylmaleimide PKC-inhibitor GF109203X efficiently modulates MRP-associated multiple drug resistance. Biochem Biophys Res Commun 1995, 206, 119-126.
145. 4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 1995, 208, 345-352.
146. van der Graaf WTA, de Vries EGE, Timmer-Bosscha H, et al. Effects of amiodarone, cyclosporin A, and PSC 833 on the cytotoxicity of mitoxanrone, doxorubicin, and vincristine in non-P-glycoprotein human small cell lung cancer cell lines. Cancer Res 1994, 54, 5368-5373.
147. Versantvoort CHM, Schuurhuis GJ, Pinedo HM, et al. Genistein modulates the decreased drug accumulation in non-P-glycoprotein mediated multidrug resistant tumour cells. Br J Cancer 1993, 68, 939-946.
148. Gollapudi S, Thadepalli F, Kim CH, Gupta S. Difloxacin reverses multidrug resistance in HL-60/AR cells that overexpress the multidrug resistance-related protein (MRP) gene. Oncol Res 1995, 7, 73-85.
149. Griffith OW, Meister A. Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J Biol Chem 1979, 254, 7558-7560.
150. Mans DRA, Schuurhuis GJ, Treskes M, et al. Modulation by D, L-buthionine-S,R-sulphoximine of etoposide cytotoxicity on human non-small cell lung, ovarian and breast carcinoma cell lines. Eur J Cancer 1992, 28A, 1447-1452.
151. Lutzky J, Astor MB, Taub RN, et al. Role of glutathione and dependent enzymes in anthracycline-resistant HL60/AR cells. Cancer Res 1989, 49, 4120-4125.
152. Meijer C, Mulder NH, Timmer-Bosscha H, Peters WHM, de Vries EGE. Combined in vitro modulation of adriamycin resistance. Int J Cancer 1991, 49, 582-586.
153. Deneke SM, Fanburg BL. Regulation of cellular glutathione. Am J Physiol 1989, 257, L163-L173.
154. Meister A, Anderson ME. Glutathione. Annu Rev Biochem 1983, 52, 711-760.
155. Crooke ST. Therapeutic applications of oligonucleotides. Annu Rev Pharmacol Toxicol 1992, 32, 329-376.
156. Crooke RM. In vitro toxicology and pharmacokinetics of antisense oligonucleotides. Anticancer Drug Res 1991, 6, 609-646.
157. Stewart AJ, Canitrot Y, Baracchini E, Dean NM, Deeley RG, Cole SPC. Reduction of expression of the multidrug resistance protein, MRP, in human tumor cells by antisense phosphorothioate oligonucleotides. Biochem Pharmacol 1996, 51, 461-469.
158. Futscher BW, Abbaszadegan MR, Domann F, Dalton WS. Analysis of MRP mRNA in mitoxantrone-selected, multidrug-resistant human tumor cells. Biochem Pharmacol 1994, 47, 1601-1606.
159. Lazaruk LC, Campling BG, Baer KA, et al. Drug resistance and expression of MRP and MDR1 in small cell lung cancer cell lines. Proc Am Assoc Cancer Res 1995, 36, 1953.
160. Chan HSL, Haddad G, Hipfher DR, Deeley RG, Cole SPC. Sensitive detection of the multidrug resistance protein (MRP) in malignant cells. Proc Am Assoc Cancer Res 1995, 36, 326.
161. Nooter K, Westerman AM, Flens MJ, et al. Expression of the multidrug resistance-associated protein (MRP) gene in human cancers. Clin Cancer Res 1995, 1, 1301-1310.
162. Nooter K, Bosman FT, Burger H, et al. Expression of the multidrug resistance-associated protein (MRP) gene in primary non-small-cell lung cancer. Ann Oncol 1996, 7, 75-81.
163. Twentyman PR, Rhodes T, Rayner S. A comparison of rhodamine 123 accumulation and efflux in cells with P-glycoprotein-mediated and MRP-associated multidrug resistance pheno-types. Eur J Cancer 1994, 30A, 1360-1369.
164. Feller N, Kuiper CM, Lankelma J, et al. Functional detection of MDR1/P170 and MRP/P190 mediated multidrug resistance in tumor cells by flow cytometry. Br J Cancer 1996, 72, 543-549.
165. Neyfakh AA. Use of fluorescent dyes as molecular probes for the study of multidrug resistance. Exp Cell Res 1988, 174, 168-176.
166. Homolya L, Hollo Z, Germann UA, Pastan I, Gottesman MM, Sarkadi B. Fluorescent cellular indicators are extruded by the multidrug resistance protein. J Biol Chem 1993, 268, 21493-21496.
167. Feller N, Broxterman HJ, Wahrer DCR, Pinedo HM. ATP-dependent efflux of calcein by the multidrug resistance protein (MRP): no inhibition by intracellular glutathione depletion. FEBS Lett 1995, 368, 385-388.
168. Zimniak P, Awasthi YC. ATP-dependent transport systems for organic anions. Hepatology 1993, 17, 330-339.
169. Sugawara I, Aria T, Yamashita T, Yoshida A, Masunaga S, Itoyama S. Expression of multidrug resistance-associated protein (MRP) in anaplastic carcinoma of the thyroid. Cancer Lett 1994, 82, 185-188.
170. Abe T, Hasegawa S, Taniguchi K, et al. Possible involvement of multidrug-resistance-associated protein (MRP) gene expression in spontaneous drug resistance to vincristine, etoposide, and adriamycin in human glioma cells. Int J Cancer 1995, 58, 860-864.
171. Bordow SB, Haber M, Madafiglio J, Cheung B, Marshall GM, Norris MD. Expression of the multidrug resistance-associated protein (MRP) gene correlates with amplification and overexpression of the N-myc oncogene in childhood neuroblastoma. Cancer Res 1994, 54, 5036-5040.
172. Norris MD, Bordow SB, Marshall GM, Haber PS, Cohn SL, Haber M. Expression of the multidrug resistance-associated protein (MRP) and outcome in patients with neuroblastoma. N Engl J Med 1996, 334, 231-238.
173. Doyle LA, Ross DD, Ordonez JV, et al. An etoposide-resistant lung cancer subline overexpresses the multidrug resistance-associated protein. Br J Cancer 1995, 72, 535-542.
174. Barrand MA, Heppel-Parton AC, Wright KA, Rabbitts PH, Twentyman PR. A 190-kilodalton protein overexpressed in non-P-glycoprotein-containing multidrug-resistant cells and its relationship to the MRP gene. J Natl Cancer Inst 1994, 86, 110-117.
175. Sumizawa T, Chuman Y, Sakamoto H, et al. Non-P-glycoprotein-mediated multidrug-resistant human KB cells selected in medium containing adriamycin, cepharanthine, and mezerein. Somat Cell Mol Genet 1994, 20, 423-435.
176. Gaj CL, Anyanwutaku IO, Cole SPC, Chang Y, Cheng YC. Reversal of multidrug resistance associated protein mediated multidrug resistance in a human
177. Schneider E, Horton JK, Yang C-H, Nakagawa M, Cowan KH. Multidrug resistance-associated protein gene overexpression and reduced drug sensitivity of topoisomerase II in a human breast carcinoma MCF7 cell line selected for etoposide resistance. Cancer Res 1994, 54, 152-158.
178. Benchekroun MN, Schneider E, Safa AR, Townsend AJ, Sinha BK. Mechanisms of resistance to ansamycin antibioics in human breast cancer cell lines. Mol Pharmacol 1994, 46, 677-684.
179. Kim W-J, Kakehi Y, Hirai M, et al. Multidrug resistance-associated protein-mediated multidrug resistance modulated by cyclosporin A in a human bladder cancer cell line. Jpn J Cancer Res 1995, 86, 969-977.
180. Lorico A, Rappa G, Srimatkandada S, et al. Increased rate of adenosine triphosphate-dependent etoposide (VP-16) efflux in a murine leukemia cell line overexpressing the multidrug resistance-associated protein (MRP) gene. Cancer Res 1995, 55, 4352-4360.
181. Burger H, Nooter K, Zaman GJR, et al. Expression of the multidrug resistance-associated protein (MRP) in acute and chronic leukemias. Leukemia 1994, 8, 990-997.
182. Schuurhuis GJ, Broxterman HJ, Ossenkoppele GJ, et al. Functional multidrug resistance phenotype associated with combined overexpression of Pgp/MDR1 and MRP together with 1-β-D-arabinofuranosylcytosine sensitivity may predict clinical response in acute myeloid leukemia. Clin Cancer Res 1995, 1, 81-93.
183. Burger H, Nooter K, Sonneveld P, van Wingerden KE, Zaman GJR, Stoter G. High expression of the multidrug resistance-associated protein (MRP) in chronic and prolymphocytic leukemia. Br J Haematol 1994, 88, 348-356.
184. Beck J, Niethammer D, Gekeler V. High mdr1- and mrp-, but low topoisomerase IIα-gene expression in B-cell chronic lymphocytic leukaemias. Cancer Lett 1994, 86, 135-142.
185. Hart SM, Ganeshaguru K, Hoffbrand AV, Prentice HG, Mehta AB. Expression of the multidrug resistance-associated protein (MRP) in acute leukemia. Leukemia 1994, 8, 2163-2168.
186. Ross DD, Doyle LA, Schiffer CA, et al. Expression of multidrug resistance-associated protein (MRP) mRNA in blast cells from acute myeloid leukemia (AML) patients. Leukemia 1996, 10, 48-55.
187. Nooter K, Burger H, Stoter G. Multidrug resistance-associated protein (MRP) in haematological malignancies. Leukaem Lymph 1995, 18, 179-184.
188. Ota E, Abe Y, Oshika Y, et al. Expression of the multidrug resistance-associated protein (MRP) gene in non-small-cell lung cancer. Br J Cancer 1995, 72, 550-554.