Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane

Hepatology

Volumn 38, Issue 2, 2003, Pages 374-384

  Rius, Maria ^b   Nies, Anne T ^b   Hummel Eisenbeiss, Johanna ^b   Jedlitschky, Gabriele ^b   Keppler, Dietrich ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BILE SALT; CARRIER PROTEIN; CHOLIC ACID; CYSTEINE; GLUTATHIONE; GLYCOCHOLIC ACID; MULTIDRUG RESISTANCE PROTEIN 4; QUINOLINE DERIVATIVE; VERLUKAST;

ARTICLE; BILE SECRETION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOLOCALIZATION; LIVER CELL; MEMBRANE TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 0042766881     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1053/jhep.2003.50331     Document Type: Article

References (44)

1. Hofmann AF, Sjovall J, Kurz G, Radominska A, Schteingart CD, Tint GS, Vlahceric ZR, et al. A proposed nomenclature for bile acids. J Lipid Res 1992;33:599-604.
2. Kaplowitz N, Aw TY, Ookhtens M. The regulation of hepatic glutathione. Annu Rev Pharmacol Toxicol 1985;25:715-744.
3. Sies H, Bartoli GM, Burk RF, Waydhas C. Glutathione efflux from perfused rat liver after phenobarbital treatment, during drug oxidations, and in selenium deficiency. Eur J Biochem 1978;89:113-118.
4. Akerboom TP, Bilzer M, Sies H. The relationship of biliary glutathione disulfide efflux and intracellular glutathione disulfide content in perfused rat liver. J Biol Chem 1982;257:4248-4252.
5. Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol 2000;62:649-671.
6. Loe DW, Almquist KC, Deeley RG, Cole SP. Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 1996;271:9675-9682.
7. Loe DW, Deeley RG, Cole SP. Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 2000;293:530-538.
8. Paulusma CC, van Geer MA, Evers R, Heijn M, Ottenhoff R, Borst P, Oude Elferink RP. Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione. Biochem J 1999;338:393-401.
9. Büchler M, König J, Brom M, Kartenbeck J, Spring H, Horie T, Keppler D. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 1996;271:15091-15098.
10. Keppler D, König J, Nies AT. Conjugate export pumps of the multidrug resistance protein (MRP) family in liver. In: Arias IM, Boyer JL, Chisari FV, Fausto N, Schachter D, Shafritz DA, eds. The Liver: Biology and Pathology. New York: Lippincott Williams & Wilkins, 2001:373-382.
11. Li L, Lee TK, Meier PJ, Ballatori N. Identification of glutathione as a driving force and leukotriene C4 as a substrate for oatp1, the hepatic sinusoidal organic solute transporter. J Biol Chem 1998;273:16184-16191.
12. Lee K, Belinsky MG, Bell DW, Testa JR, Kruh GD. Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/canalicular multispecific organic anion transporter-related transporter. Cancer Res 1998;58:2741-2747.
13. Schuetz JD, Connelly MC, Sun D, Paibir SG, Flynn PM, Srinivas RV, Kumar A, et al. MRP4: A previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat Med 1999;5:1048-1051.
14. Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 2000;92:1295-1302.
15. Lai L, Tan TM. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem J 2002;361:497-503.
16. van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 2002;13:595-603.
17. Wielinga PR, Reid G, Challa EE, van dH I, van Deemter L, de Haas M, Mol C, et al. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharm 2002;62:1321-1331.
18. Schuetz EG, Strom S, Yasuda K, Lecureur V, Assem M, Brimer C, Lamba J, et al. Disrupted bile acid homeostasis reveals an unexpected interaction among nuclear hormone receptors, transporters, and cytochrome P450. J Biol Chem 2001;276:39411-39418.
19. Lee K, Klein-Szanto AJ, Kruh GD. Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells. J Natl Cancer Inst 2000;92:1934-1940.
20. Hirrlinger J, König J, Dringen R. Expression of mRNAs of multidrug resistance proteins (Mrps) in cultured rat astrocytes, oligodendrocytes, microglial cells and neurones. J Neurochem 2002;82:716-719.
21. Zelcer N, Reid G, Wielinga PR, Kuil AJ, van der Heijden, Schuetz JD, Borst P. Steroid- and bile acid-conjugates are substrates of human MRP4 (ABCC4). Biochem J 2003;371:361-367.
22. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJ, Juijn JA, Baas F, et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res 1997;57:3537-3547.
23. Chen ZS, Lee K, Kruh GD. Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 2001;276:33747-33754.
24. Chen ZS, Lee K, Walther S, Raftogianis RB, Kuwano M, Zeng H, Kruh GD. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 2002;62:3144-3150.
25. Adachi M, Sampath J, Lan LB, Sun D, Hargrove P, Flatley R, Tatum A, et al. Expression of MRP4 confers resistance to ganciclovir and compromises bystander cell killing. J Biol Chem 2002;277:38998-39004.
26. Hirohashi T, Suzuki H, Takikawa H, Sugiyama Y. ATP-dependent transport of bile salts by rat multidrug resistance-associated protein 3 (Mrp3). J Biol Chem 2000;275:2905-2910.
27. Akita H, Suzuki H, Sugiyama Y. Sinusoidal efflux of taurocholate correlates with the hepatic expression level of Mrp3. Biochem Biophys Res Commun 2002;299:681-687.
28. Mayer R, Kartenbeck J, Büchler 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.
29. Cui Y, König J, Buchholz JK, Spring H, Leier I, Keppler D. Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 1999;55:929-937.
30. Böhme M, Müller M, Leier I, Jedlitschky G, Keppler D. Cholestasis caused by inhibition of the adenosine triphosphate-dependent bile salt transport in rat liver. Gastroenterology 1994;107:255-265.
31. Keppler D, Jedlitschky G, Leier I. Transport function and substrate specificity of multidrug resistance protein. Methods Enzymol 1998;292:607-616.
32. Leier I, Jedlitschky G, Buchholz U, Keppler D. Characterization of the ATP-dependent leukotriene C4 export carrier in mastocycoma cells. Eur J Biochem 1994;220:599-606.
33. Donner MG, Keppler D. Up-regulation of basolateral multidrug resistance protein 3 (Mrp3) in cholestatic rat liver. HEPATOLOGY 2001;34:351-359.
34. Nies AT, König J, Pfannschmidt M, Klat E, Hofmann WJ, Keppler D. Expression of the multidrug resistance proteins MRP2 and MRP3 in human hepatocellular carcinoma. Int J Cancer 2001;94:492-499.
35. Nies AT, Spring H, Thon WF, Keppler D, Jedlitschky G. Immunolocalization of multidrug resistance protein 5 in the human genitourinary system. J Urology 2002;167:2271-2275.
36. Jedlitschky G, Butchell B, Keppler D. The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J Biol Chem 2000;275:30069-30074.
37. König J, Cui Y, Nies AT, Keppler D. A novel human organic anion transporting polypeptide localized to the basolateral hepatocyce membrane. Am J Physiol Gastrointest Liver Physiol 2000;278:G156-G164.
38. Sormunen R, Eskelinen S, Lehto VP. Bile canaliculus formation in cultured HEPG2 cells. Lab Invest 1993;68:652-662.
39. Cantz T, Nies AT, Brom M, Hofmann AF, Keppler D. MRP2, a human conjugate export pump, is present and transports fluo 3 into apical vacuoles of Hep G2 cells. Am J Physiol Gastrointest Liver Physiol 2000;278:G522-G531.
40. Loe DW, Deeley RG, Cole SP. Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 1998;58:5130-5136.
41. Noe J, Stieger B, Meier PJ. Functional expression of the canalicular bile salt export pump of human liver. Gastroenterology 2002;123:1659-1666.
42. Kipp H, Arias IM. Trafficking of canalicular ABC transporters in hepatocytes. Annu Rev Physiol 2002;64:595-608.
43. Lee TK, Hammond CL, Ballatori N. Intracellular glutathione regulates taurocholate transport in HepG2 cells. Toxicol Appl Pharmacol 2001;174: 207-215.
44. Hagenbuch B, Meier PJ. The superfamily of organic anion transporting polypeptides. Biochim Biophys Acta 2003;1609:1-18.