Biochemistry and Pharmacology of Human ABCC1/MRP1 and Its Role in Detoxification and in Multidrug Resistance of Cancer Chemotherapy

Recent Advances in Cancer Research and Therapy

Volumn , Issue , 2012, Pages 371-404

  Mo, Wei ^a   Liu, Jing Yuan ^a   Zhang, Jian Ting ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882563406     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-397833-2.00014-5     Document Type: Chapter

References (194)

1. J.T. Zhang (2007) Use of arrays to investigate the contribution of ATP-binding cassette transporters to drug resistance in cancer chemotherapy and prediction of chemosensitivity. Cell Res 17 311-323.
2. M. Richard, R. Drouin and A.D. Beaulieu (1998) ABC50, a novel human ATP-binding cassette protein found in tumor necrosis factor-alpha-stimulated synoviocytes. Genomics 53 137-145.
3. D. Barthelme, U. Scheele, S. Dinkelaker, et al. (2007) Structural organization of essential iron–sulfur clusters in the evolutionarily highly conserved ATP-binding cassette protein ABCE1. J Biol Chem 282 14598-14607.
4. I.D. Kerr (2004) Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 315 166-173.
5. S.P. Cole, G. Bhardwaj, J.H. Gerlach, et al. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line [see comments]. Science 258 1650-1654.
6. M.L. Slovak, J.P. Ho, S.P. Cole, et al. (1995) The LRP gene encoding a major vault protein associated with drug resistance maps proximal to MRP on chromosome 16: evidence that chromosome breakage plays a key role in MRP or LRP gene amplification. Cancer Res 55 4214-4219.
7. E. Bakos, T. Hegedus, Z. Hollo, et al. (1996) Membrane topology and glycosylation of the human multidrug resistance-associated protein. J Biol Chem 271 12322-12326.
8. D.R. Hipfner, K.C. Almquist, E.M. Leslie, et al. (1997) Membrane topology of the multidrug resistance protein (MRP). A study of glycosylation-site mutants reveals an extracytosolic NH2 terminus. J Biol Chem 272 23623-23630.
9. C. Kast and P. Gros (1997) Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immunofluorescence. J Biol Chem 272 26479-26487.
10. C. Kast and P. Gros (1998) Epitope insertion favors a six transmembrane domain model for the carboxy-terminal portion of the multidrug resistance-associated protein. Biochemistry 37 2305-2313.
11. J.T. Zhang (2000) Determinant of the extracellular location of the N-terminus of human multidrug-resistance-associated protein. Biochem J 348 597-606.
12. J. Lipp, N. Flint, M.T. Haeuptle, et al. (1989) Structural requirements for membrane assembly of proteins spanning the membrane several times. J Cell Biol 109 2013-2022.
13. N. Liu and D.T. Brown (1993) Transient translocation of the cytoplasmic (endo) domain of a type I membrane glycoprotein into cellular membranes. J Cell Biol 120 877-883.
14. Q. Chen, Y. Yang, Y. Liu, et al. (2002) Cytoplasmic retraction of the amino terminus of human multidrug resistance protein 1. Biochemistry 41 9052-9062.
15. Q. Chen, Y. Yang, L. Li, et al. (2006) The amino terminus of the human multidrug resistance transporter ABCC1 has a U-shaped folding with a gating function. J Biol Chem 281 31152-31163.
16. M. Muller, M. Yong, X.H. Peng, et al. (2002) Evidence for the role of glycosylation in accessibility of the extracellular domains of human MRP1 (ABCC1). Biochemistry 41 10123-10132.
17. P.Y. Chou and G.D. Fasman (1978) Empirical predictions of protein conformation. Annu Rev Biochem 47 251-276.
18. P.Y. Chou and G.D. Fasman (1979) Prediction of beta-turns. Biophys J 26 367-373.
19. M.F. Rosenberg, Q. Mao, A. Holzenburg, et al. (2001) The Structure of the Multidrug Resistance Protein 1 (MRP1/ABCC1). Crystallization and single-particle analysis. J Biol Chem 276 16076-16082.
20. G. Chang (2003) Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J Mol Biol 330 419-430.
21. G. Chang and C.B. Roth (2001) Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293 1793-1800.
22. J.D. Campbell, K. Koike, C. Moreau, et al. (2004) Molecular modeling correctly predicts the functional importance of Phe594 in transmembrane helix 11 of the multidrug resistance protein, MRP1 (ABCC1). J Biol Chem 279 463-468.
23. R.J. Dawson and K.P. Locher (2006) Structure of a bacterial multidrug ABC transporter. Nature 443 180-185.
24. G. Chang, C.B. Roth, C.L. Reyes, et al. (2006) Retraction. Science 314 1875.
25. M.K. DeGorter, G. Conseil, R.G. Deeley, et al. (2008) Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem Biophys Res Commun 365 29-34.
26. W. Mo and J.T. Zhang (2009) Oligomerization of human ATP-binding cassette transporters and its potential significance in human disease. Expert Opin Drug Metab Toxicol 5 1049-1063.
27. J. Xu, Y. Liu, Y. Yang, et al. (2004) Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J Biol Chem 279 19781-19789.
28. C.A. McDevitt, R.F. Collins, M. Conway, et al. (2006) Purification and 3D structural analysis of oligomeric human multidrug transporter ABCG2. Structure 14 1623-1632.
29. L. Jette, M. Potier and R. Beliveau (1997) P-glycoprotein is a dimer in the kidney and brain capillary membranes: effect of cyclosporin A and SDZ-PSC 833. Biochemistry 36 13929-13937.
30. M. Naito and T. Tsuruo (1992) Functionally active homodimer of P-glycoprotein in multidrug-resistant tumor cells. Biochem Biophys Res Commun 185 284-290.
31. M.S. Poruchynsky and V. Ling (1994) Detection of oligomeric and monomeric forms of P-glycoprotein in multidrug resistant cells [published erratum appears in Biochemistry 1994 Aug 2;33(30):9032]. Biochemistry 33 4163-4174.
32. S.G. Aller, J. Yu, A. Ward, et al. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323 1718-1722.
33. M. Soszynski, A. Kaluzna, B. Rychlik, et al. (1998) Radiation inactivation suggests that human multidrug resistance-associated protein 1 occurs as a dimer in the human erythrocyte membrane. Arch Biochem Biophys 354 311-316.
34. Y. Yang, Y. Liu, Z. Dong, et al. (2007) Regulation of function by dimerization through the amino-terminal membrane-spanning domain of human ABCC1/MRP1. J Biol Chem 282 8821-8830.
35. D. Schrenk, P.R. Baus, N. Ermel, et al. (2001) Up-regulation of transporters of the MRP family by drugs and toxins. Toxicol Lett 120 51-57.
36. G.M. Su, M.W. Davey and R.A. Davey (1998) Induction of broad drug resistance in small cell lung cancer cells and its reversal by paclitaxel. Int J Cancer 76 702-708.
37. Y. Yamane, M. Furuichi, R. Song, et al. (1998) Expression of multidrug resistance protein/GS-X pump and gamma-glutamylcysteine synthetase genes is regulated by oxidative stress. J Biol Chem 273 31075-31085.
38. Y.C. Lin-Lee, S. Tatebe, N. Savaraj, et al. (2001) Differential sensitivities of the MRP gene family and gamma-glutamylcysteine synthetase to prooxidants in human colorectal carcinoma cell lines with different p53 status. Biochem Pharmacol 61 555-563.
39. R.M. Harvie, M.W. Davey and R.A. Davey (1997) Increased MRP expression is associated with resistance to radiation, anthracyclines and etoposide in cells treated with fractionated gamma-radiation. Int J Cancer 73 164-167.
40. L. Vernhet, A. Courtois, N. Allain, et al. (1999) Overexpression of the multidrug resistance-associated protein (MRP1) in human heavy metal-selected tumor cells. FEBS Lett 443 321-325.
41. S.H. Kim, H. Bark and C.H. Choi (2005) Mercury induces multidrug resistance-associated protein gene through p38 mitogen-activated protein kinase. Toxicol Lett 155 143-150.
42. E.W. Eijdems, M. De Haas, J.M. Coco-Martin, et al. (1995) Mechanisms of MRP overexpression in four human lung-cancer cell lines and analysis of the MRP amplicon. Int J Cancer 60 676-684.
43. K. Yasui, S. Mihara, C. Zhao, et al. (2004) Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res 64 1403-1410.
44. M. Golalipour, F. Mahjoubi, M.H. Sanati, et al. (2007) Gene dosage is not responsible for the upregulation of MRP1 gene expression in adult leukemia patients. Arch Med Res 38 297-304.
45. Q. Zhu and M.S. Center (1994) Cloning and sequence analysis of the promoter region of the MRP gene of HL60 cells isolated for resistance to adriamycin. Cancer Res 54 4488-4492.
46. Q. Zhu and M.S. Center (1996) Evidence that SP1 modulates transcriptional activity of the multidrug resistance-associated protein gene. DNA Cell Biol 15 105-111.
47. Q. Wang and W.T. Beck (1998) Transcriptional suppression of multidrug resistance-associated protein (MRP) gene expression by wild-type p53. Cancer Res 58 5762-5769.
48. E.U. Kurz, S.P. Cole and R.G. Deeley (2001) Identification of DNA–protein interactions in the 5΄ flanking and 5΄ untranslated regions of the human multidrug resistance protein (MRP1) gene: evaluation of a putative antioxidant response element/AP-1 binding site. Biochem Biophys Res Commun 285 981-990.
49. M.T. Osborn and T.C. Chambers (1996) Role of the stress-activated/c-Jun NH2-terminal protein kinase pathway in the cellular response to adriamycin and other chemotherapeutic drugs. J Biol Chem 271 30950-30955.
50. C. Shinoda, M. Maruyama, T. Fujishita, et al. (2005) Doxorubicin induces expression of multidrug resistance-associated protein 1 in human small cell lung cancer cell lines by the c-jun N-terminal kinase pathway. Int J Cancer 117 21-31.
51. U. Stein, K. Jurchott, W. Walther, et al. (2001) Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. J Biol Chem 276 28562-28569.
52. Y. Yang, Q. Chen and J.T. Zhang (2002) Structural and functional consequences of mutating cysteine residues in the amino terminus of human multidrug resistance-associated protein 1. J Biol Chem 277 44268-44277.
53. K. Ito, K.E. Weigl, R.G. Deeley, et al. (2003) Mutation of proline residues in the NH(2)-terminal region of the multidrug resistance protein, MRP1 (ABCC1): effects on protein expression, membrane localization, and transport function. Biochim Biophys Acta 1615 103-114.
54. E. Bakos, R. Evers, G. Szakacs, et al. (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273 32167-32175.
55. C.J. Westlake, S.P. Cole and R.G. Deeley (2005) Role of the NH2-terminal membrane spanning domain of multidrug resistance protein 1/ABCC1 in protein processing and trafficking. Mol Biol Cell 16 2483-2492.
56. E. Bakos, R. Evers, G. Calenda, et al. (2000) Characterization of the amino-terminal regions in the human multidrug resistance protein (MRP1). J Cell Sci 113 4451-4461.
57. C.J. Westlake, Y.M. Qian, M. Gao, et al. (2003) Identification of the structural and functional boundaries of the multidrug resistance protein 1 cytoplasmic loop 3. Biochemistry 42 14099-14113.
58. A.T. Nies, J. Konig, Y. Cui, et al. (2002) Structural requirements for the apical sorting of human multidrug resistance protein 2 (ABCC2). Eur J Biochem 269 1866-1876.
59. N. Sharma, A. Crane, J.P. Clement J.P.t., et al. (1999) The C terminus of SUR1 is required for trafficking of KATP channels. J Biol Chem 274 20628-20632.
60. C.J. Westlake, L. Payen, M. Gao, et al. (2004) Identification and characterization of functionally important elements in the multidrug resistance protein 1 COOH-terminal region. J Biol Chem 279 53571-53583.
61. Y.-M. Qian, W. Qiu, M. Gao, et al. (2001) Characterization of binding of leukotriene C4 by human multidrug resistance protein 1. Evidence of differential interactions with NH2- and COOH-proximal halves of the protein. J Biol Chem 276 38636-38644.
62. J. Karwatsky, M. Leimanis, J. Cai, et al. (2005) The leucotriene C4 binding sites in multidrug resistance protein 1 (ABCC1) include the first membrane multiple spanning domain. Biochemistry 44 340-351.
63. J. Karwatsky, R. Daoud, J. Cai, et al. (2003) Binding of a photoaffinity analogue of glutathione to MRP1 (ABCC1) within two cytoplasmic regions (L0 and L1) as well as transmembrane domains 10-11 and 16-17. Biochemistry 42 3286-3294.
64. Y.M. Qian, C.E. Grant, C.J. Westlake, et al. (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.
65. X.Q. Ren, T. Furukawa, S. Aoki, et al. (2001) Glutathione-dependent binding of a photoaffinity analog of agosterol A to the C-terminal half of human multidrug resistance protein. J Biol Chem 276 23197-23206.
66. Q. Mao, W. Qiu, K.E. Weigl, et al. (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.
67. R. Daoud, J. Desneves, L.W. Deady, et al. (2000) The multidrug resistance protein is photoaffinity labeled by a quinoline-based drug at multiple sites. Biochemistry 39 6094-6102.
68. R. Daoud, M. Julien, P. Gros, et al. (2001) Major photoaffinity drug binding sites in multidrug resistance protein 1 (MRP1) are within transmembrane domains 10-11 and 16-17. J Biol Chem 276 12324-12330.
69. D.W. Loe, K.C. Almquist, R.G. Deeley, et al. (1996) Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 271 9675-9682.
70. P. Wu, C.J. Oleschuk, Q. Mao, et al. (2005) Analysis of human multidrug resistance protein 1 (ABCC1) by matrix-assisted laser desorption ionization/time of flight mass spectrometry: toward identification of leukotriene C4 binding sites. Mol Pharmacol 68 1455-1465.
71. M. Gao, H.R. Cui, D.W. Loe, et al. (2000) Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J Biol Chem 275 13098-13108.
72. A. Kern, Z. Szentpetery, K. Liliom, et al. (2004) Nucleotides and transported substrates modulate different steps of the ATPase catalytic cycle of MRP1 multidrug transporter. Biochem J 380 549-560.
73. K. Nagata, M. Nishitani, M. Matsuo, et al. (2000) Nonequivalent nucleotide trapping in the two nucleotide binding folds of the human multidrug resistance protein MRP1. J Biol Chem 275 17626-17630.
74. Y. Hou, L. Cui, J.R. Riordan, et al. (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J Biol Chem 275 20280-20287.
75. Y.X. Hou, J.R. Riordan and X.B. Chang (2003) ATP binding, not hydrolysis, at the first nucleotide-binding domain of multidrug resistance-associated protein MRP1 enhances ADP.Vi trapping at the second domain. J Biol Chem 278 3599-3605.
76. J. Renes, E.E. de Vries, G.J. Hooiveld, et al. (2000) Multidrug resistance protein MRP1 protects against the toxicity of the major lipid peroxidation product 4-hydroxynonenal. Biochem J 350 555-561.
77. G. Jedlitschky, I. Leier, U. Buchholz, et al. (1994) ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res 54 4833-4836.
78. I. Leier, G. Jedlitschky, U. Buchholz, et al. (1994) The MRP gene encodes an ATP-dependent export pump for lekotriene C4 and structurally related conjugates. J Biol Chem 269 27807-27810.
79. R. Evers, N.H. Cnubben, J. Wijnholds, et al. (1997) Transport of glutathione prostaglandin A conjugates by the multidrug resistance protein 1. FEBS Lett 419 112-116.
80. C.M. Paumi, M. Wright, A.J. Townsend, et al. (2003) Multidrug resistance protein (MRP) 1 and MRP3 attenuate cytotoxic and transactivating effects of the cyclopentenone prostaglandin, 15-deoxy-Delta(12,14)prostaglandin J2 in MCF7 breast cancer cells. Biochemistry 42 5429-5437.
81. G. Jedlitschky, I. Leier, U. Buchholz, et al. (1997) ATP-dependent transport of bilirubin glucuronides by the multidrug resistance protein MRP1 and its hepatocyte canalicular isoform MRP2. Biochem J 327 305-310.
82. D.W. Loe, K.C. Almquist, S.P. Cole, et al. (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.
83. G. Jedlitschky, I. Leier, U. Buchholz, et al. (1996) Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res 56 988-994.
84. Y.M. Qian, W.C. Song, H. Cui, et al. (2001) Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276 6404-6411.
85. K. Barnouin, I. Leier, G. Jedlitschky, et al. (1998) Multidrug resistance protein-mediated transport of chlorambucil and melphalan conjugated to glutathione. Br J Cancer 77 201-209.
86. S.P. Cole, K.E. Sparks, K. Fraser, et al. (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54 5902-5910.
87. M.J. Grzywacz, J.M. Yang and W.N. Hait (2003) Effect of the multidrug resistance protein on the transport of the antiandrogen flutamide. Cancer Res 63 2492-2498.
88. M.E. Smeets, R.A. Raymakers, G. Vierwinden, et al. (1999) Idarubicin DNA intercalation is reduced by MRP1 and not Pgp. Leukemia 13 1390-1398.
89. F. Innocenti, D.L. Kroetz, E. Schuetz, et al. (2009) Comprehensive pharmacogenetic analysis of irinotecan neutropenia and pharmacokinetics. J Clin Oncol 27 2604-2614.
90. O. Janneh, E. Jones, B. Chandler, et al. (2007) Inhibition of P-glycoprotein and multidrug resistance-associated proteins modulates the intracellular concentration of lopinavir in cultured CD4 T cells and primary human lymphocytes. J Antimicrob Chemother 60 987-993.
91. E.R. Meaden, P.G. Hoggard, P. Newton, et al. (2002) P-glycoprotein and MRP1 expression and reduced ritonavir and saquinavir accumulation in HIV-infected individuals. J Antimicrob Chemother 50 583-588.
92. A.L. Dogan, O. Legrand, A.M. Faussat, et al. (2004) Evaluation and comparison of MRP1 activity with three fluorescent dyes and three modulators in leukemic cell lines. Leuk Res 28 619-622.
93. D.F. Robbiani, R.A. Finch, D. Jager, et al. (2000) The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103 757-768.
94. J. Jin and A.T. Jones (2009) The pH sensitive probe 5-(and-6)-carboxyl seminaphthorhodafluor is a substrate for the multidrug resistance-related protein MRP1. Int J Cancer 124 233-238.
95. B. Rychlik, A. Balcerczyk, A. Klimczak, et al. (2003) The role of multidrug resistance protein 1 (MRP1) in transport of fluorescent anions across the human erythrocyte membrane. J Membr Biol 193 79-90.
96. Y.G. Assaraf, L. Rothem, J.H. Hooijberg, et al. (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.
97. M. Stark, L. Rothem, G. Jansen, et al. (2003) Antifolate resistance associated with loss of MRP1 expression and function in Chinese hamster ovary cells with markedly impaired export of folate and cholate. Mol Pharmacol 64 220-227.
98. H. Zeng, Z.S. Chen, M.G. Belinsky, et al. (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.
99. J.H. Hooijberg, H.J. Broxterman, M. Kool, et al. (1999) Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res 59 2532-2535.
100. E.M. Leslie, K. Ito, P. Upadhyaya, et al. (2001) 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.
101. D.W. Loe, R.K. Stewart, T.E. Massey, et al. (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.
102. T.E. Tribull, R.H. Bruner and L.J. Bain (2003) The multidrug resistance-associated protein 1 transports methoxychlor and protects the seminiferous epithelium from injury. Toxicol Lett 142 61-70.
103. P. Mitra, C.A. Oskeritzian, S.G. Payne, et al. (2006) Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci USA 103 16394-16399.
104. H. Suzuki and Y. Sugiyama (1998) Excretion of GSSG and glutathione conjugates mediated by MRP1 and cMOAT/MRP2. Semin Liver Dis 18 359-376.
105. I. Tamai, J. Yamashita, Y. Kido, et al. (2000) Limited distribution of new quinolone antibacterial agents into brain caused by multiple efflux transporters at the blood–brain barrier. J Pharmacol Exp Ther 295 146-152.
106. J. Wijnholds, R. Evers, M.R. van Leusden, et al. (1997) Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3 1275-1279.
107. C.E. Grant, G. Valdimarsson, D.R. Hipfner, et al. (1994) Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res 54 357-361.
108. G.C. Williams, A. Liu, G. Knipp, et al. (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.
109. D.P. Olson, D.T. Scadden, R.T. D’Aquila, et al. (2002) The protease inhibitor ritonavir inhibits the functional activity of the multidrug resistance related-protein 1 (MRP-1). AIDS 16 1743-1747.
110. R.G. Deeley and S.P. Cole (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 580 1103-1111.
111. D.W. Loe, R.G. Deeley and S.P. Cole (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.
112. J. Renes, E.G. de Vries, E.F. Nienhuis, et al. (1999) ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br J Pharmacol 126 681-688.
113. D.W. Loe, R.G. Deeley and S.P. Cole (2000) Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 293 530-538.
114. E.M. Leslie, R.J. Bowers, R.G. Deeley, et al. (2003) Structural requirements for functional interaction of glutathione tripeptide analogs with the human multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 304 643-653.
115. S. Aoki, Z.S. Chen, K. Higasiyama, et al. (2001) Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn J Cancer Res 92 886-895.
116. Z. Hollo, L. Homolya, T. Hegedus, et al. (1996) Transport properties of the multidrug resistance-associated protein (MRP) in human tumour cells. FEBS Lett 383 99-104.
117. R.W. Robey, S. Shukla, E.M. Finley, et al. (2008) Inhibition of P-glycoprotein (ABCB1)- and multidrug resistance-associated protein 1 (ABCC1)-mediated transport by the orally administered inhibitor, CBT-1((R)). Biochem Pharmacol 75 1302-1312.
118. L.Y. Tao, Y.J. Liang, F. Wang, et al. (2009) Cediranib (recentin, AZD2171) reverses ABCB1- and ABCC1-mediated multidrug resistance by inhibition of their transport function. Cancer Chemother Pharmacol 64 961-969.
119. M. Bobrowska-Hagerstrand, A. Wrobel, L. Mrowczynska, et al. (2003) Flavonoids as inhibitors of MRP1-like efflux activity in human erythrocytes. A structure–activity relationship study. Oncol Res 13 463-469.
120. V. Gekeler, R. Boer, W. Ise, et al. (1995) The specific bisindolylmaleimide PKC-inhibitor GF 109203X efficiently modulates MRP-associated multiple drug resistance. Biochem Biophys Res Commun 206 119-126.
121. R. Abdul-Ghani, V. Serra, B. Gyorffy, et al. (2006) The PI3K inhibitor LY294002 blocks drug export from resistant colon carcinoma cells overexpressing MRP1. Oncogene 25 1743-1752.
122. D. Peer and R. Margalit (2006) Fluoxetine and reversal of multidrug resistance. Cancer Lett 237 180-187.
123. V. Gekeler, W. Ise, K.H. Sanders, et al. (1995) The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208 345-352.
124. B. Lania-Pietrzak, K. Michalak, A.B. Hendrich, et al. (2005) Modulation of MRP1 protein transport by plant, and synthetically modified flavonoids. Life Sci 77 1879-1891.
125. D. Trompier, X.B. Chang, R. Barattin, et al. (2004) Verapamil and its derivative trigger apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res 64 4950-4956.
126. T. Sumizawa, Z.S. Chen, Y. Chuman, et al. (1997) Reversal of multidrug resistance-associated protein-mediated drug resistance by the pyridine analog PAK-104P. Mol Pharmacol 51 399-405.
127. L.S. Zheng, F. Wang, Y.H. Li, et al. (2009) Vandetanib (Zactima, ZD6474) antagonizes ABCC1- and ABCG2-mediated multidrug resistance by inhibition of their transport function. PLoS One 4 e5172.
128. R.A. Peck, J. Hewett, M.W. Harding, et al. (2001) Phase I and pharmacokinetic study of the novel MDR1 and MRP1 inhibitor biricodar administered alone and in combination with doxorubicin. J Clin Oncol 19 3130-3141.
129. B.H. Norman, J.M. Gruber, S.P. Hollinshead, et al. (2002) Tricyclic isoxazoles are novel inhibitors of the multidrug resistance protein (MRP1). Bioorg Med Chem Lett 12 883-886.
130. A.J. Stewart, Y. Canitrot, E. Baracchini, et al. (1996) Reduction of expression of the multidrug resistance protein (MRP) in human tumor cells by antisense phosphorothioate oligonucleotides. Biochem Pharmacol 51 461-469.
131. C. Erlichman, S.A. Boerner, C.G. Hallgren, et al. (2001) The HER tyrosine kinase inhibitor CI1033 enhances cytotoxicity of 7-ethyl-10-hydroxycamptothecin and topotecan by inhibiting breast cancer resistance protein-mediated drug efflux. Cancer Res 61 739-748.
132. C. Ozvegy-Laczka, T. Hegedus, G. Varady, et al. (2004) High-affinity interaction of tyrosine kinase inhibitors with the ABCG2 multidrug transporter. Mol Pharmacol 65 1485-1495.
133. P.J. Houghton, G.S. Germain, F.C. Harwood, et al. (2004) Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro. Cancer Res 64 2333-2337.
134. J. Xu, H. Peng and J.T. Zhang (2007) Human multidrug transporter ABCG2, a target for sensitizing drug resistance in cancer chemotherapy. Curr Med Chem 14 689-701.
135. A.H. Dantzig, R.L. Shepard, S.E. Pratt, et al. (2004) Evaluation of the binding of the tricyclic isoxazole photoaffinity label LY475776 to multidrug resistance associated protein 1 (MRP1) orthologs and several ATP-binding cassette (ABC) drug transporters. Biochem Pharmacol 67 1111-1121.
136. H. Osada, T. Tokunaga, Y. Abe, et al. (2003) Reversal of drug resistance mediated by hammerhead ribozyme against multidrug resistance-associated protein 1 in a human glioma cell line. Int J Oncol 22 823-827.
137. W. Niewiarowski, E. Gendaszewska, G. Rebowski, et al. (2000) Multidrug resistance-associated protein—reduction of expression in human leukaemia cells by antisense phosphorothioate olignucleotides. Acta Biochim Pol 47 1183-1188.
138. A.E. Peaston, M. Gardaneh, A.V. Franco, et al. (2001) MRP1 gene expression level regulates the death and differentiation response of neuroblastoma cells. Br J Cancer 85 1564-1571.
139. B.J. Kuss, M. Corbo, W.M. Lau, et al. (2002) In vitro and in vivo downregulation of MRP1 by antisense oligonucleotides: a potential role in neuroblastoma therapy. Int J Cancer 98 128-133.
140. M.J. Flens, G.J. Zaman, P. van der Valk, et al. (1996) Tissue distribution of the multidrug resistance protein. Am J Pathol 148 1237-1247.
141. E. Bakos and L. Homolya (2007) Portrait of multifaceted transporter, the multidrug resistance-associated protein 1 (MRP1/ABCC1). Pflugers Arch 453 621-641.
142. V.V. Rao, J.L. Dahlheimer, M.E. Bardgett, et al. (1999) Choroid plexus epithelial expression of MDR1 P glycoprotein and multidrug resistance-associated protein contribute to the blood–cerebrospinal-fluid drug-permeability barrier. Proc Natl Acad Sci USA 96 3900-3905.
143. S.R. Wright, A.H. Boag, G. Valdimarsson, et al. (1998) Immunohistochemical detection of multidrug resistance protein in human lung cancer and normal lung. Clin Cancer Res 4 2279-2289.
144. A. Rajagopal and S.M. Simon (2003) Subcellular localization and activity of multidrug resistance proteins. Mol Biol Cell 14 3389-3399.
145. F. Gennuso, C. Fernetti, C. Tirolo, et al. (2004) Bilirubin protects astrocytes from its own toxicity by inducing up-regulation and translocation of multidrug resistance-associated protein 1 (Mrp1). Proc Natl Acad Sci USA 101 2470-2475.
146. A. Lorico, G. Rappa, R.A. Finch, et al. (1997) Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res 57 5238-5242.
147. Y.J. Lee, H. Kusuhara and Y. Sugiyama (2004) Do multidrug resistance-associated protein-1 and -2 play any role in the elimination of estradiol-17 beta-glucuronide and 2,4-dinitrophenyl-S-glutathione across the blood–cerebrospinal fluid barrier? J Pharm Sci 93 99-107.
148. E.M. Leslie, R.G. Deeley and S.P. Cole (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204 216-237.
149. D. Sugiyama, H. Kusuhara, Y.J. Lee, et al. (2003) Involvement of multidrug resistance associated protein 1 (Mrp1) in the efflux transport of 17beta estradiol-d-17beta-glucuronide (E217betaG) across the blood–brain barrier. Pharm Res 20 1394-1400.
150. J. Wijnholds, G.L. Scheffer, M. van der Valk, et al. (1998) Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med 188 797-808.
151. J. Hirrlinger, J. Konig, D. Keppler, et al. (2001) The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J Neurochem 76 627-636.
152. C.F. Mueller, J.D. Widder, J.S. McNally, et al. (2005) The role of the multidrug resistance protein-1 in modulation of endothelial cell oxidative stress. Circ Res 97 637-644.
153. S. Zochbauer-Muller, M. Filipits, M. Rudas, et al. (2001) P-glycoprotein and MRP1 expression in axillary lymph node metastases of breast cancer patients. Anticancer Res 21 119-124.
154. G.F. Sullivan, P.S. Amenta, J.D. Villanueva, et al. (1998) The expression of drug resistance gene products during the progression of human prostate cancer. Clin Cancer Res 4 1393-1403.
155. F. Mahjoubi, M. Golalipour, A. Ghavamzadeh, et al. (2008) Expression of MRP1 gene in acute leukemia. Sao Paulo Med J 126 172-179.
156. M. Kourti, N. Vavatsi, N. Gombakis, et al. (2007) Expression of multidrug resistance 1 (MDR1), multidrug resistance-related protein 1 (MRP1), lung resistance protein (LRP), and breast cancer resistance protein (BCRP) genes and clinical outcome in childhood acute lymphoblastic leukemia. Int J Hematol 86 166-173.
157. S.L. Plasschaert, E.S. de Bont, M. Boezen, et al. (2005) Expression of multidrug resistance-associated proteins predicts prognosis in childhood and adult acute lymphoblastic leukemia. Clin Cancer Res 11 8661-8668.
158. D.P. Olson, B.J. Taylor, M. La, et al. (2005) The prognostic significance of P-glycoprotein, multidrug resistance-related protein 1 and lung resistance protein in pediatric acute lymphoblastic leukemia: a retrospective study of 295 newly diagnosed patients by the Children’s Oncology Group. Leuk Lymphoma 46 681-691.
159. S.L. Plasschaert, E. Vellenga, E.S. de Bont, et al. (2003) High functional P-glycoprotein activity is more often present in T-cell acute lymphoblastic leukaemic cells in adults than in children. Leuk Lymphoma 44 85-95.
160. A. Tafuri, C. Gregorj, M.T. Petrucci, et al. (2002) MDR1 protein expression is an independent predictor of complete remission in newly diagnosed adult acute lymphoblastic leukemia. Blood 100 974-981.
161. J.H. Do, S.H. Oh, E.J. Song, et al. (2007) Treatment outcome of multidrug resistance related mRNA expression and c-jun-N-terminal kinase activity in patients with acute myeloid leukemia. Korean J Lab Med 27 229-236.
162. M.M. van den Heuvel-Eibrink, B. van der Holt, A.K. Burnett, et al. (2007) CD34-related coexpression of MDR1 and BCRP indicates a clinically resistant phenotype in patients with acute myeloid leukemia (AML) of older age. Ann Hematol 86 329-337.
163. B. Laupeze, L. Amiot, B. Drenou, et al. (2002) High multidrug resistance protein activity in acute myeloid leukaemias is associated with poor response to chemotherapy and reduced patient survival. Br J Haematol 116 834-838.
164. N. Ohno, A. Tani, Z.S. Chen, et al. (2001) Prognostic significance of multidrug resistance protein in adult T-cell leukemia. Clin Cancer Res 7 3120-3126.
165. J.E. Diestra, E. Condom, X.G. Del Muro, et al. (2003) Expression of multidrug resistance proteins P-glycoprotein, multidrug resistance protein 1, breast cancer resistance protein and lung resistance related protein in locally advanced bladder cancer treated with neoadjuvant chemotherapy: biological and clinical implications. J Urol 170 1383-1387.
166. C. Atalay, A. Demirkazik and U. Gunduz (2008) Role of ABCB1 and ABCC1 gene induction on survival in locally advanced breast cancer. J Chemother 20 734-739.
167. L. Moureau-Zabotto, S. Ricci, J.P. Lefranc, et al. (2006) Prognostic impact of multidrug resistance gene expression on the management of breast cancer in the context of adjuvant therapy based on a series of 171 patients. Br J Cancer 94 473-480.
168. M. Filipits, G. Pohl, M. Rudas, et al. (2005) Clinical role of multidrug resistance protein 1 expression in chemotherapy resistance in early-stage breast cancer: the Austrian Breast and Colorectal Cancer Study Group. J Clin Oncol 23 1161-1168.
169. H. Burger, J.A. Foekens, M.P. Look, et al. (2003) RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clin Cancer Res 9 827-836.
170. R. Langer, K. Specht, K. Becker, et al. (2005) Association of pretherapeutic expression of chemotherapy-related genes with response to neoadjuvant chemotherapy in Barrett carcinoma. Clin Cancer Res 11 7462-7469.
171. M. Filipits, U. Jaeger, I. Simonitsch, et al. (2000) Clinical relevance of the lung resistance protein in diffuse large B-cell lymphomas. Clin Cancer Res 6 3417-3423.
172. M. Ohsawa, Y. Ikura, H. Fukushima, et al. (2005) Immunohistochemical expression of multidrug resistance proteins as a predictor of poor response to chemotherapy and prognosis in patients with nodal diffuse large B-cell lymphoma. Oncology 68 422-431.
173. Y. Soini, K. Jarvinen, R. Kaarteenaho-Wiik, et al. (2001) The expression of P-glycoprotein and multidrug resistance proteins 1 and 2 (MRP1 and MRP2) in human malignant mesothelioma. Ann Oncol 12 1239-1245.
174. N. Larbcharoensub, J. Leopairat, E. Sirachainan, et al. (2008) Association between multidrug resistance-associated protein 1 and poor prognosis in patients with nasopharyngeal carcinoma treated with radiotherapy and concurrent chemotherapy. Hum Pathol 39 837-845.
175. M. Haber, J. Smith, S.B. Bordow, et al. (2006) Association of high-level MRP1 expression with poor clinical outcome in a large prospective study of primary neuroblastoma. J Clin Oncol 24 1546-1553.
176. P. de Cremoux, N. Jourdan-Da-Silva, J. Couturier, et al. (2007) Role of chemotherapy resistance genes in outcome of neuroblastoma. Pediatr Blood Cancer 48 311-317.
177. H. Goto, N. Keshelava, K.K. Matthay, et al. (2000) Multidrug resistance-associated protein 1 (MRP1) expression in neuroblastoma cell lines and primary tumors. Med Pediatr Oncol 35 619-622.
178. M. Filipits, V. Haddad, K. Schmid, et al. (2007) Multidrug resistance proteins do not predict benefit of adjuvant chemotherapy in patients with completely resected non-small cell lung cancer: International Adjuvant Lung Cancer Trial Biologic Program. Clin Cancer Res 13 3892-3898.
179. W. Berger, U. Setinek, P. Hollaus, et al. (2005) Multidrug resistance markers P-glycoprotein, multidrug resistance protein 1, and lung resistance protein in non-small cell lung cancer: prognostic implications. J Cancer Res Clin Oncol 131 355-363.
180. K. Yoh, G. Ishii, T. Yokose, et al. (2004) Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 10 1691-1697.
181. A. Faggad, S. Darb-Esfahani, R. Wirtz, et al. (2009) Expression of multidrug resistance-associated protein 1 in invasive ovarian carcinoma: implication for prognosis. Histopathology 54 657-666.
182. Y. Ohishi, Y. Oda, T. Uchiumi, et al. (2002) ATP-binding cassette superfamily transporter gene expression in human primary ovarian carcinoma. Clin Cancer Res 8 3767-3775.
183. H.J. Arts, D. Katsaros, E.G. de Vries, et al. (1999) Drug resistance-associated markers P-glycoprotein, multidrug resistance-associated protein 1, multidrug resistance-associated protein 2, and lung resistance protein as prognostic factors in ovarian carcinoma. Clin Cancer Res 5 2798-2805.
184. Y.H. Kim, G. Ishii, K. Goto, et al. (2009) Expression of breast cancer resistance protein is associated with a poor clinical outcome in patients with small-cell lung cancer. Lung Cancer 65 105-111.
185. J.J. Yeh, N.Y. Hsu, W.H. Hsu, et al. (2005) Comparison of chemotherapy response with P-glycoprotein, multidrug resistance-related protein-1, and lung resistance-related protein expression in untreated small cell lung cancer. Lung 183 177-183.
186. A.J. Zurita, J.E. Diestra, E. Condom, et al. (2003) Lung resistance-related protein as a predictor of clinical outcome in advanced testicular germ-cell tumours. Br J Cancer 88 879-886.
187. E. Ota, Y. Abe, Y. Oshika, et al. (1995) Expression of the multidrug resistance-associated protein (MRP) gene in non-small-cell lung cancer. Br J Cancer 72 550-554.
188. Y. Oshika, M. Nakamura, T. Tokunaga, et al. (1998) Multidrug resistance-associated protein and mutant p53 protein expression in non-small cell lung cancer. Mod Pathol 11 1059-1063.
189. N. Triller, P. Korosec, I. Kern, et al. (2006) Multidrug resistance in small cell lung cancer: expression of P-glycoprotein, multidrug resistance protein 1 and lung resistance protein in chemo-naive patients and in relapsed disease. Lung Cancer 54 235-240.
190. K. Nooter, G. Brutel de la Riviere, M.P. Look, et al. (1997) The prognostic significance of expression of the multidrug resistance-associated protein (MRP) in primary breast cancer. Br J Cancer 76 486-493.
191. K. Nooter, G.B. de la Riviere, J. Klijn, et al. (1997) Multidrug resistance protein in recurrent breast cancer. Lancet 349 1885-1886.
192. M.D. Norris, S.B. Bordow, G.M. Marshall, et al. (1996) Expression of the gene for multidrug-resistance-associated protein and outcome in patients with neuroblastoma. N Engl J Med 334 231-238.
193. P. Bader, F. Schilling, M. Schlaud, et al. (1999) Expression analysis of multidrug resistance associated genes in neuroblastomas. Oncol Rep 6 1143-1146.
194. T. Matsunaga, H. Shirasawa, T. Hishiki, et al. (1998) Expression of MRP and cMOAT in childhood neuroblastomas and malignant liver tumors and its relevance to clinical behavior. Jpn J Cancer Res 89 1276-1283.