Mechanistic differences between GSH transport by multidrug resistance protein 1 (MRP1/ABCC1) and GSH modulation of MRP1-mediated Transport

Molecular Pharmacology

Volumn 74, Issue 6, 2008, Pages 1630-1640

  Rothnie, Alice ^a,b   Conseil, Gwenaëlle ^a   Lau, Andrea Y T ^a   Deeley, Roger G ^a   Cole, Susan P C ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; ESTRONE SULFATE; GLUTATHIONE; GLUTATHIONE DERIVATIVE; MULTIDRUG RESISTANCE PROTEIN 1; VERAPAMIL; VINCRISTINE;

ARTICLE; CONFORMATIONAL TRANSITION; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG TRANSPORT; HUMAN; HUMAN CELL; HYDROLYSIS; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATE; APIGENIN; AZIDES; BINDING SITES; BINDING, COMPETITIVE; CELL LINE, TUMOR; ESTRONE; GLUTATHIONE; HUMANS; HYDROLYSIS; LEUKOTRIENE C4; P-GLYCOPROTEIN; PHOSPHORUS RADIOISOTOPES; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VERAPAMIL; VINCRISTINE;

EID: 57349196661     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.108.049080     Document Type: Article

References (40)

1. Bakos E, Evers R, Sinkó E, Váradi A, Borst P, and Sarkadi B (2000) Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol Pharmacol 57:760-768.
2. Bakos E, Evers R, Szakács G, Tusnády GE, Welker E, Szabó K, de Haas M, van Deemter L, Borst P, Váradi A, et al. (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273:32167-32175.
3. Chang XB, Hou YX, and Riordan JR (1997) ATPase activity of purified multidrug resistance-associated protein. J Biol Chem 272:30962- 30968.
4. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, and Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650-1654.
5. Cole SP and Deeley RG (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 27:438-446.
6. Conseil G, Deeley RG, and Cole SP (2006) 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 281:43-50.
7. Dawson RJ and Locher KP (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581:935-938.
8. Deeley RG, Westlake C, and Cole SP (2006) Transmembrane transport of endo- and xenobiotics by membrane ATP-binding cassette multidrug resistance proteins. Physiol Rev 86:849-899.
9. DeGorter MK, Conseil G, Deeley RG, Campbell RL, and Cole SP (2008) Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem Biophys Res Commun 365:29-34.
10. Gao M, Cui HR, Loe DW, Grant CE, Almquist KC, Cole SP, and Deeley RG (2000) Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J Biol Chem 275:13098-13108.
11. Haimeur A, Conseil G, Deeley RG, and Cole SP (2004) The MRP-related and BCRP/ ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr Drug Metab 5:21-53.
12. Hipfner DR, Almquist KC, Stride BD, Deeley RG, and Cole SP (1996) Location of a protease-hypersensitive region in the multidrug resistance protein (MRP) by mapping of the epitope of MRP-specific monoclonal antibody QCRL-1. Cancer Res 56:3307-3314.
13. Hipfner DR, Gao M, Scheffer G, Scheper RJ, Deeley RG, and Cole SP (1998) Epitope mapping of monoclonal antibodies specific for the 190-kDa multidrug resistance protein (MRP). Br J Cancer 78:1134-1140.
14. Hooijberg JH, Pinedo HM, Vrasdonk C, Priebe W, Lankelma J, and Broxterman HJ (2000) The effect of glutathione on the ATPase activity of MRP1 in its natural membranes. FEBS Lett 469:47-51.
15. Hou Y, Cui L, Riordan JR, and Chang X (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein 1. J Biol Chem 275:20280-20287.
16. Jedlitschky G, Leier I, Buchholz U, Barnouin K, Kurz G, and Keppler D (1996) Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res 56:988-994.
17. Leier I, Jedlitschky G, Buchholz U, Center M, Cole SP, Deeley RG, and Keppler D (1996) ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem J 314:433-437.
18. Leslie EM, Bowers RJ, Deeley RG, and Cole SP (2003a) Structural requirements for functional interaction of glutathione tripeptide analogs with the human multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 304:643-653.
19. Leslie EM, Deeley RG, and Cole SP (2003b) Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab Dispos 31:11-15.
20. Leslie EM, Deeley RG, and Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216-237.
21. Leslie EM, Ito K, Upadhyaya P, Hecht SS, Deeley RG, and Cole SP (2001a) 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 276:27846-27854.
22. Leslie EM, Mao Q, Oleschuk CJ, Deeley RG, and Cole SP (2001b) Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol Pharmacol 59:1171-1180.
23. Létourneau IJ, Nakajima A, Deeley RG, and Cole SP (2008) Role of proline 1150 in functional interactions between the membrane spanning domains and nucleotide binding domains of the MRP1 (ABCC1) transporter. Biochem Pharmacol 75:1659-1669.
24. Loe DW, Almquist KC, Cole SP, and Deeley RG (1996a) ATP-dependent 17 β-estradiol 17-(β-D-glucuronide) transport by multidrug resistance protein (MRP). Inhibition by cholestatic steroids. J Biol Chem 271:9683-9689.
25. 4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 271:9675-9682.
26. Loe DW, Deeley RG, and Cole SP (1998) Characterization of vincristine transport by the Mr 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58:5130-5136.
27. Loe DW, Deeley RG, and Cole SP (2000) Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 293:530-538.
28. Manciu L, Chang XB, Buyse F, Hou YX, Gustot A, Riordan JR, and Ruysschaert JM (2003) Intermediate structural states involved in MRP1-mediated drug transport. Role of glutathione. J Biol Chem 278:3347-3356.
29. Mao QC, Leslie EM, Deeley RG, and Cole SP (1999) ATPase activity of purified and reconstituted multidrug resistance protein MRP1 from drug-selected H69AR cells. Biochim Biophys Acta 1461:69-82.
30. Morrow CS, Peklak-Scott C, Bishwokarma B, Kute TE, Smitherman PK, and Townsend AJ (2006) Multidrug resistance protein 1 (MRP1, ABCC1) mediates resistance to mitoxantrone via glutathione-dependent drug efflux. Mol Pharmacol 69:1499-1505.
31. Nagata K, Nishitani M, Matsuo M, Kioka N, Amachi T, and Ueda K (2000) Nonequivalent nucleotide trapping in the two nucleotide binding folds of the human multidrug resistance protein MRP1. J Biol Chem 275:17626- 17630.
32. Qian YM, Song WC, Cui H, Cole SP, and Deeley RG (2001) Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276: 6404-6411.
33. Ren XQ, Furukawa T, Nakajima Y, Takahashi H, Aoki S, Sumizawa T, Haraguchi M, Kobayashi M, Chijiiwa K, and Akiyama S (2005) GSH inhibits trypsinization of the C-terminal half of human MRP1. J Biol Chem 280:6231-6237.
34. Rothnie A, Callaghan R, Deeley RG, and Cole SP (2006) Role of GSH in estrone sulfate binding and translocation by the multidrug resistance protein 1 (MRP1/ ABCC1). J Biol Chem 281:13906-13914.
35. Taguchi Y, Yoshida A, Takada Y, Komano T, and Ueda K (1997) Anti-cancer drugs and glutathione stimulate vanadate-induced trapping of nucleotide in multidrug resistance-associated protein (MRP). FEBS Lett 401:11-14.
36. Tanford C (1983) Translocation pathway in the catalysis of active-transport. Proc Natl Acad Sci U S A 80:3701-3705.
37. Urbatsch IL, Sankaran B, Weber J, and Senior AE (1995) P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J Biol Chem 270:19383-19390.
38. Wijnholds J, deLange EC, Scheffer GL, van den Berg DJ, Mol CA, van der Valk M, Schinkel AH, Scheper RJ, Breimer DD, and Borst P (2000) Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 105:279-285.
39. Wijnholds J, Evers R, van Leusden MR, Mol CA, Zaman GJ, Mayer U, Beijnen JH, van der Valk M, Krimpenfort P, and Borst P (1997) Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3:1275-1279.
40. Yang R, McBride A, Hou YX, Goldberg A, and Chang XB (2005) Nucleotide dissociation from NBD1 promotes solute transport by MRP1. Biochim Biophys Acta 1668:248-261.