Regulation of the function of the human ABCG2 multidrug transporter by cholesterol and bile acids: Effects of mutations in potential substrate and steroid binding sites

Drug Metabolism and Disposition

Volumn 42, Issue 4, 2014, Pages 575-585

  Telbisz, Ágnes ^a   Hegedüs, Csilla ^b   Váradi, András ^a   Sarkadi, Balázs ^a   Özvegy Laczka, Csilla ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BILE ACID; BREAST CANCER RESISTANCE PROTEIN; CHOLESTEROL; MULTIDRUG RESISTANCE PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROLYSIS; INSECT CELL; LIPID TRANSPORT; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SF9 CELL; STEROID BINDING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; BILE CANALICULI; BINDING SITES; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CHOLESTEROL; HEPATOCYTES; HUMANS; NEOPLASM PROTEINS; POINT MUTATION; SF9 CELLS; SPODOPTERA; SUBSTRATE SPECIFICITY; TRANSFECTION; XENOBIOTICS;

EID: 84896140722     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.113.055731     Document Type: Article

References (32)

1. Allen JD, van Loevezijn A, Lakhai JM, van der Valk M, van Tellingen O, Reid G, Schellens JH, Koomen GJ, and Schinkel AH (2002) Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 1:417-425.
2. 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. (Pubitemid 30183717)
3. Blazquez AG, Briz O, Romero MR, Rosales R, Monte MJ, Vaquero J, Macias RI, Cassio D, and Marin JJ (2012) Characterization of the role of ABCG2 as a bile acid transporter in liver and placenta. Mol Pharmacol 81:273-283.
4. Bodo A, Bakos E, Szeri F, Varadi A, and Sarkadi B (2003) Differential modulation of the human liver conjugate transporters MRP2 and MRP3 by bile acids and organic anions. J Biol Chem 278:23529-23537. (Pubitemid 36830172)
5. Garrigues A, Escargueil AE, and Orlowski S (2002) The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci USA 99:10347-10352.
6. Hegedus C, Szakács G, Homolya L, Orbán TI, Telbisz A, Jani M, and Sarkadi B (2009) Ins and outs of the ABCG2 multidrug transporter: an update on in vitro functional assays. Adv Drug Deliv Rev 61:47-56.
7. Im YJ, Raychaudhuri S, Prinz WA, and Hurley JH (2005) Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437:154-158. (Pubitemid 41613443)
8. Imai Y, Asada S, Tsukahara S, Ishikawa E, Tsuruo T, and Sugimoto Y (2003) Breast cancer resistance protein exports sulfated estrogens but not free estrogens. Mol Pharmacol 64:610-618. (Pubitemid 37048564)
9. Janvilisri T, Shahi S, Venter H, Balakrishnan L, and van Veen HW (2005) Arginine-482 is not essential for transport of antibiotics, primary bile acids and unconjugated sterols by the human breast cancer resistance protein (ABCG2). Biochem J 385:419-426. (Pubitemid 40165074)
10. Jigorel E, Le Vee M, Boursier-Neyret C, Parmentier Y, and Fardel O (2006) Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab Dispos 34:1756-1763. (Pubitemid 44427479)
11. Kerr ID, Haider AJ, and Gelissen IC (2011) The ABCG family of membrane-associated transporters: you don't have to be big to be mighty. Br J Pharmacol 164:1767-1779.
12. Kimura Y, Kioka N, Kato H, Matsuo M, and Ueda K (2007a) Modulation of drug-stimulated ATPase activity of human MDR1/P-glycoprotein by cholesterol. Biochem J 401:597-605. (Pubitemid 46166441)
13. Kimura Y, Kodan A, Matsuo M, and Ueda K (2007b) Cholesterol fill-in model: mechanism for substrate recognition by ABC proteins. J Bioenerg Biomembr 39:447-452.
14. Li T and Chiang JY (2012) Bile acid signaling in liver metabolism and diseases. J Lipids 2012:754067.
15. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, and Schellens JH (2001) Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 61:3458-3464. (Pubitemid 32695041)
16. Mennone A, Soroka CJ, Harry KM, and Boyer JL (2010) Role of breast cancer resistance protein in the adaptive response to cholestasis. Drug Metab Dispos 38:1673-1678.
17. Ozvegy-Laczka C, Hegedus T, Várady G, Ujhelly O, Schuetz JD, Váradi A, Kéri G, Orfi L, Német K, and Sarkadi B (2004) High-affinity interaction of tyrosine kinase inhibitors with the ABCG2 multidrug transporter. Mol Pharmacol 65:1485-1495. (Pubitemid 38668306)
18. Ozvegy-Laczka C, Köblös G, Sarkadi B, and Váradi A (2005) Single amino acid (482) variants of the ABCG2 multidrug transporter: major differences in transport capacity and substrate recognition. Biochim Biophys Acta 1668:53-63. (Pubitemid 40164733)
19. Ozvegy-Laczka C, Laczkó R, Hegedus C, Litman T, Várady G, Goda K, Hegedus T, Dokholyan NV, Sorrentino BP, and Váradi A, et al. (2008) Interaction with the 5D3 monoclonal antibody is regulated by intramolecular rearrangements but not by covalent dimer formation of the human ABCG2 multidrug transporter. J Biol Chem 283:26059-26070.
20. Ozvegy C, Litman T, Szakács G, Nagy Z, Bates S, Váradi A, and Sarkadi B (2001) Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem Biophys Res Commun 285:111-117. (Pubitemid 32912517)
21. Ozvegy C, Váradi A, and Sarkadi B (2002) Characterization of drug transport, ATP hydrolysis, and nucleotide trapping by the human ABCG2 multidrug transporter. Modulation of substrate specificity by a point mutation. J Biol Chem 277:47980-47990. (Pubitemid 35470743)
22. Pál A, Méhn D, Molnár E, Gedey S, Mészáros P, Nagy T, Glavinas H, Janáky T, von Richter O, and Báthori G, et al. (2007) Cholesterol potentiates ABCG2 activity in a heterologous expression system: improved in vitro model to study function of human ABCG2. J Pharmacol Exp Ther 321:1085-1094. (Pubitemid 46762703)
23. Robey RW, To KK, Polgar O, Dohse M, Fetsch P, Dean M, and Bates SE (2009) ABCG2: a perspective. Adv Drug Deliv Rev 61:3-13.
24. Simonović BR and Momirovićc M (1997) Determination of critical micelle concentration of bile acid salts by micro-calorimetric titration. Mikrochim Acta 127:101-104 DOI:10.1007/BF01243172.
25. Storch CH, Ehehalt R, Haefeli WE, and Weiss J (2007) Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro. J Pharmacol Exp Ther 323:257-264. (Pubitemid 47443266)
26. Suzuki M, Suzuki H, Sugimoto Y, and Sugiyama Y (2003) ABCG2 transports sulfated conjugates of steroids and xenobiotics. J Biol Chem 278:22644-22649. (Pubitemid 36830322)
27. Telbisz A, Müller M, Ozvegy-Laczka C, Homolya L, Szente L, Váradi A, and Sarkadi B (2007) Membrane cholesterol selectively modulates the activity of the human ABCG2 multidrug transporter. Biochim Biophys Acta 1768:2698-2713. (Pubitemid 350081032)
28. Telbisz A, Özvegy-Laczka C, Heged}us T, Váradi A, and Sarkadi B (2013) Effects of the lipid environment, cholesterol and bile acids on the function of the purified and reconstituted human ABCG2 protein. Biochem J 450:387-395.
29. Vaidya SS and Gerk PM (2006) Lack of interaction between tauroursodeoxycholate and ATP-binding cassette transporter isoform G2 (ABCG2). Mol Pharm 3:303-306. (Pubitemid 44021436)
30. Velamakanni S, Janvilisri T, Shahi S, and van Veen HW (2008) A functional steroid-binding element in an ATP-binding cassette multidrug transporter. Mol Pharmacol 73:12-17. (Pubitemid 350294192)
31. Wang N, Yvan-Charvet L, Lütjohann D, Mulder M, Vanmierlo T, Kim TW, and Tall AR (2008) ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain. FASEB J 22:1073-1082. (Pubitemid 351519962)
32. Williams SP and Sigler PB (1998) Atomic structure of progesterone complexed with its receptor. Nature 393:392-396. (Pubitemid 28269716)