Transport of glutathione and glutathione conjugates by MRP1

Trends in Pharmacological Sciences

Volumn 27, Issue 8, 2006, Pages 438-446

  Cole, Susan P C ^a   Deeley, Roger G ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CARRIER PROTEIN; GLUTATHIONE; GLUTATHIONE DISULFIDE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; VINCA ALKALOID; VINCRISTINE; XENOBIOTIC AGENT;

AMINO ACID SUBSTITUTION; BINDING AFFINITY; DRUG PROTEIN BINDING; DRUG TRANSPORT; ENZYME SPECIFICITY; GLUTATHIONE METABOLISM; HUMAN; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SITE DIRECTED MUTAGENESIS;

ANIMALS; BIOLOGICAL TRANSPORT; GLUTATHIONE; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION;

EID: 33745897902     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2006.06.008     Document Type: Review

References (93)

1. Hayes J.D., et al. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 51-88
2. Jones D.C., et al. Serotonergic neurotoxic metabolites of ecstasy identified in rat brain. J. Pharmacol. Exp. Ther. 313 (2005) 422-431
3. Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17 (1992) 463-468
4. Dean M., and Allikmets R. Complete characterization of the human ABC gene family. J. Bioenerg. Biomembr. 33 (2001) 475-479
5. Hoffmann U., and Kroemer H.K. The ABC transporters MDR1 and MRP2: multiple functions in disposition of xenobiotics and drug resistance. Drug Metab. Rev. 36 (2004) 669-701
6. Ballatori N., et al. Molecular mechanisms of reduced glutathione transport: role of the MRP/CFTR/ABCC and OATP/SLC21A families of membrane proteins. Toxicol. Appl. Pharmacol. 204 (2005) 238-255
7. Leslie E.M., et al. Multidrug resistance proteins in toxicology: role of P-glycoprotein, MRP1, MRP2 and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204 (2005) 216-237
8. Haimeur A., et al. The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr. Drug Metab. 5 (2004) 21-53
9. Chen J., et al. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 12 (2003) 651-661
10. Loo T.W., et al. The LSGGQ motif in each nucleotide-binding domain of human P-glycoprotein is adjacent to the opposing Walker A sequence. J. Biol. Chem. 277 (2002) 41303-41306
11. Nagel G. Differential function of the two nucleotide binding domains on cystic fibrosis transmembrane conductance regulator. Biochim. Biophys. Acta 1461 (1999) 263-274
12. Deeley, R.G. et al. Transmembrane transport of endo- and xenobiotics by the ATP-binding cassette multidrug resistance proteins (MRPs). Physiol. Rev. (in press)
13. Binyamin L., et al. Probing ATP-dependent conformation changes in the multidrug resistance protein 1 (MRP1/ABCC1) in live tumor cells with a novel recombinant single-chain Fv antibody targeted to the extracellular N-terminus. Int. J. Cancer 116 (2005) 703-709
14. Cole S.P.C., et al. Overexpression of a transporter gene in a multidrug resistant human lung cancer cell line. Science 258 (1992) 1650-1654
15. Nies A.T., et al. Expression and immunolocalization of the multidrug resistance proteins MRP1-MRP6 (ABCC1-ABCC6) in human brain. Neuroscience 129 (2004) 349-360
16. Zhang Y., et al. Plasma membrane localization of resistance-associated protein homologs in brain capillary endothelial cells. J. Pharmacol. Exp. Ther. 311 (2004) 449-455
17. de Lange E.C. Potential role of ABC transporters as a detoxification system at the blood-CSF barrier. Adv. Drug Deliv. Rev. 56 (2004) 1793-1809
18. Wijnholds J., et al. Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J. Clin. Invest. 105 (2000) 279-285
19. Tribull T.E., et al. The multidrug resistance-associated protein 1 transports methoxychlor and protects the seminiferous epithelium from injury. Toxicol. Lett. 142 (2003) 61-70
20. Létourneau I.J., et al. Limited modulation of the transport activity of the human multidrug resistance proteins MRP1, MRP2 and MRP3 by nicotine glucuronide metabolites. Toxicol. Lett. 157 (2005) 9-19
21. 4 and structurally related conjugates. J. Biol. Chem. 269 (1994) 27807-27810
22. 4 and chemotherapeutic agents in membrane vesicles: demonstration of glutathione-dependent vincristine transport. J. Biol. Chem. 271 (1996) 9675-9682
23. Conseil G., et al. Polymorphisms of MRP1 (ABCC1) and related ATP-dependent drug transporters. Pharmacogenet Genomics 15 (2005) 523-533
24. 1 and its glutathione conjugates by the product of the MRP gene. Mol. Pharmacol. 51 (1997) 1034-1041
25. Peklak-Scott C., et al. Dynamics of glutathione conjugation and conjugate efflux in detoxification of the carcinogen, 4-nitroquinoline 1-oxide: contributions of glutathione, glutathione S-transferase, and MRP1. Biochemistry 44 (2005) 4426-4433
26. Deeley R.G., and Cole S.P.C. Substrate recognition and transport by multidrug resistance protein (MRP) 1. FEBS Lett. 580 (2006) 1103-1111
27. Norman B.H., et al. Tricyclic isoxazoles are novel inhibitors of the multidrug resistance protein (MRP1). Bioorg. Med. Chem. Lett. 12 (2002) 883-886
28. Norman B.H., et al. Cyclohexyl-linked tricyclic isoxazoles are potent and selective modulators of the multidrug resistance protein (MRP1). Bioorg. Med. Chem. Lett. 15 (2005) 5526-5530
29. Boumendjel A., et al. Anticancer multidrug resistance mediated by MRP1: recent advances in the discovery of reversal agents. Med. Res. Rev. 25 (2005) 453-472
30. Falk E., et al. Direct photoaffinity labelling of leukotriene binding sites. Eur. J. Biochem. 186 (1989) 741-747
31. Dantzig A.H., et al. 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 (2004) 1111-1121
32. Létourneau I.J., et al. Functional characterization of non-synonymous single nucleotide polymorphisms in the gene encoding human multidrug resistance protein 1 (MRP1/ABCC1). Pharmacogenet Genomics 15 (2005) 647-657
33. Conseil G., et al. Functional importance of three basic residues clustered at the cytosolic interface of transmembrane helix 15 in the multidrug and organic anion transporter MRP1 (ABCC1). J. Biol. Chem. 281 (2006) 43-50
34. Rosenberg M.F., et al. The structure of the multidrug resistance protein 1 (MRP1/ABCC1): crystallization and single-particle analysis. J. Biol. Chem. 276 (2001) 16076-16082
35. Manciu L., et al. Intermediate structural states involved in MRP1-mediated drug transport: role of glutathione. J. Biol. Chem. 278 (2003) 3347-3356
36. 4 binding sites. Mol. Pharmacol. 68 (2005) 1455-1465
37. Ramaen O., et al. Attempts to characterize the NBD heterodimer of MRP1: transient complex formation involves Gly771 of the ABC signature sequence but does not enhance the intrinsic ATPase activity. Biochem. J. 391 (2005) 481-490
38. Campbell J.D., et al. Molecular modeling correctly predicts the functional importance of Phe594 in transmembrane helix 11 of the multidrug resistance protein, MRP1 (ABCC1). J. Biol. Chem. 279 (2004) 463-468
39. Koike K., et al. Multiple membrane associated tryptophan residues contribute to the transport activity and substrate specificity of the human multidrug resistance protein, MRP1. J. Biol. Chem. 277 (2002) 49495-49503
40. Situ D., et al. Mutational analysis of ionisable residues proximal to the cytoplasmic interface of membrane spanning domain 3 of the multidrug resistance protein, MRP1 (ABCC1): Glutamate 1204 is important for both the expression and catalytic activity of the transporter. J. Biol. Chem. 279 (2004) 38871-38880
41. 4 or estadiol-17 (β-d-glucuronate). Biochem. Pharmacol. 70 (2005) 1056-1065
42. Haimeur A., et al. Charged amino acids in the sixth transmembrane helix of multidrug resistance protein 1 (MRP1/ABCC1) are critical determinants of transport activity. J. Biol. Chem. 277 (2002) 41326-41333
43. Haimeur A., et al. Mutations of charged amino acids in or proximal to the transmembrane helices of the second membrane spanning domain differentially affect the substrate specificity and transport activity of the multidrug resistance protein MRP1 (ABCC1). Mol. Pharmacol. 65 (2004) 1375-1385
44. Leslie E.M., et al. Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1): evidence that a triglutathione conjugate is required. J. Biol. Chem. 279 (2004) 32700-32708
45. Bao X., et al. Membrane transport proteins with complete replacement of transmembrane helices with polyalanine sequences remain functional. J. Biol. Chem. 280 (2005) 8647-8650
46. Rappa G., et al. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 57 (1997) 5232-5237
47. Loe D.W., et al. Characterization of vincristine transport by the 190 kDa multidrug resistance protein, MRP: evidence for co-transport with reduced glutathione. Cancer Res. 58 (1998) 5130-5136
48. Mao Q., et al. Functional reconstitution of substrate transport by purified multidrug resistance protein MRP1 (ABCC1) in phospholipid vesicles. J. Biol. Chem. 275 (2000) 34166-34172
49. Paumi C.M., et al. Role of the multidrug resistance protein 1 (MRP1) and glutathione S-transferase A1-1 in alkylating agent resistance. Kinetics of glutathione conjugate formation and efflux govern differential cellular sensitivity to chlorambucil versus melphalan toxicity. J. Biol. Chem. 276 (2001) 7952-7956
50. Schneider E., et al. Buthionine sulphoximine-mediated sensitisation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer 71 (1995) 738-743
51. Lorico A., et al. 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 (1997) 5238-5242
52. Hammond C.L., et al. Novel roles for glutathione in gene expression, cell death, and membrane transport of organic solutes. J. Hepatol. 34 (2001) 946-954
53. Trompier D., et al. Verapamil and its derivative trigger apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res. 64 (2004) 4950-4956
54. Hammond C.L., et al. Activation of plasma membrane reduced glutathione transport in death receptor apoptosis of HepG2 cells. Toxicol. Appl. Pharmacol. 195 (2004) 12-22
55. Hirrlinger J., et al. The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J. Neurochem. 76 (2001) 627-636
56. Mueller C.F., et al. The role of the multidrug resistance protein 1 in modulation of endothelial cell oxidative stress. Circ. Res. 97 (2005) 637-644
57. Pulaski L., et al. Identification of the multidrug-resistance protein (MRP) as the glutathione-S-conjugate export pump of erythrocytes. Eur. J. Biochem. 241 (1996) 644-648
58. Minich T., et al. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J. Neurochem. 97 (2006) 373-384
59. Loe D.W., et al. Verapamil stimulates glutathione transport by the 190 kDa multidrug resistance protein, MRP1. J. Pharmacol. Exp. Ther. 293 (2000) 530-538
60. Leslie E.M., et al. Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol. Pharmacol. 59 (2001) 1171-1180
61. Leslie E.M., et al. Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab. Dispos. 31 (2003) 11-15
62. Qian Y.M., et al. Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J. Biol. Chem. 276 (2001) 6404-6411
63. Leslie E.M., et al. Transport of the β-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 (2001) 27846-27854
64. Zelcer N., et al. Steroid and bile acid conjugates are substrates of human multidrug resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem. J. 371 (2003) 361-367
65. Leslie E.M., et al. Structural requirements for functional interaction of glutathione tripeptide analogs with the human multidrug resistance protein 1 (MRP1). J. Pharmacol. Exp. Ther. 304 (2003) 643-653
66. Ren X.Q., et al. GSH inhibits trypsinization of the C-terminal half of human MRP1. J. Biol. Chem. 280 (2005) 6231-6237
67. Buyse F., et al. Mistargeted MRPΔF728 mutant is rescued by intracellular GSH. FEBS Lett. 578 (2004) 145-151
68. Zhan Y., and Rule G.S. Glutathione induces helical formation in the carboxy terminus of human glutathione transferase A1-1. Biochemistry 43 (2004) 7244-7254
69. 125I]LY475776: evidence of a major binding site in the COOH-proximal membrane spanning domain. J. Biol. Chem. 277 (2002) 28690-28699
70. Aoki S., et al. Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn. J. Cancer Res. 92 (2001) 886-895
71. Chen Z.S., et al. Reversal of drug resistance mediated by multidrug resistance protein (MRP) 1 by dual effects of agosterol A on MRP1 function. Int. J. Cancer 93 (2001) 107-113
72. Ren X.Q., et al. Glutathione-dependent binding of a photoaffinity analog of agosterol A to the C-terminal half of human multidrug resistance protein. J. Biol. Chem. 276 (2001) 23197-23206
73. 35S]glutathione. J. Biol. Chem. 277 (2002) 35225-35231
74. 2- and COOH-proximal halves of the protein. J. Biol. Chem. 276 (2001) 38636-38644
75. Koike K., et al. Identification of proline residues in the core cytoplasmic and transmembrane regions of multidrug resistance protein 1 (MRP1/ABCC1) important for transport function, substrate specificity, and nucleotide interactions. J. Biol. Chem. 279 (2004) 12325-12336
76. Conseil G., et al. Role of two adjacent cytoplasmic tyrosine residues in MRP1 (ABCC1) transport activity and sensitivity to sulfonylureas. Biochem. Pharmacol. 69 (2005) 451-461
77. Karwatsky J., et al. 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 (2003) 3286-3294
78. Paulusma C.C., et al. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271 (1996) 1126-1128
79. Konig J., et al. MRP2, the apical export pump for anionic conjugates. In: Holland I.B., et al. (Ed). ABC Proteins: From Bacteria to Man (2003), Elsevier 423-443
80. Qiu R., et al. ABCC2-mediated biliary transport of 4-glutathionylcyclophosphamide and its contribution to elimination of 4-hydroxycyclophosphamide in rat. J. Pharmacol. Exp. Ther. 308 (2004) 1204-1212
81. Ji B., et al. Multidrug resistance-associated protein 2 (MRP2) plays an important role in the biliary excretion of glutathione conjugates of 4-hydroxynonenal. Free Radic. Biol. Med. 33 (2002) 370-378
82. Mottino A.D., et al. Biliary secretion of glutathione in estradiol 17β-d-glucuronide-induced cholestasis. J. Pharmacol. Exp. Ther. 307 (2003) 306-313
83. Lash L.H. Role of glutathione transport processes in kidney function. Toxicol. Appl. Pharmacol. 204 (2005) 329-342
84. Lai L., and Tan T.M.C. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of CAMP and resistance to purine analogues. Biochem. J. 361 (2002) 497-503
85. Rius M., et al. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38 (2003) 374-384
86. Bai J., et al. Multidrug resistance protein 4 (MRP4/ABCC4) mediates efflux of bimane-glutathione. Int. J. Biochem. Cell Biol. 36 (2004) 247-257
87. Rius M., et al. Substrate specificity of human ABCC4 (MRP4)-mediated cotransport of bile acids and reduced glutathione. Am. J. Physiol. Gastrointest. Liver Physiol. 290 (2006) G640-G649
88. Wijnholds J., et al. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7476-7481
89. Belinsky M.G., et al. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res. 62 (2002) 6172-6177
90. 4 by human multidrug resistance protein 8 (ABCC11). Mol. Pharmacol. 67 (2005) 545-557
91. Kogan I., et al. CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J. 22 (2003) 1981-1989
92. 4 and structurally related conjugates. Vitam. Horm. 64 (2002) 153-184
93. Rothnie A., et al. Role of GSH in estrone sulfate binding and translocation by the multidrug resistance protein 1 (MRP1/ABCC1). J. Biol. Chem. 281 (2006) 13906-13914