Bile salt-stimulated phospholipid efflux mediated by ABCB4 localized in nonraft membranes

Journal of Lipid Research

Volumn 54, Issue 5, 2013, Pages 1221-1230

  Morita, Shin Ya ^a   Tsuda, Tadanori ^b   Horikami, Manami ^b   Teraoka, Reiko ^b   Kitagawa, Shuji ^b   Terada, Tomohiro ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE HOSPITAL   (Japan)

^b KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

ABC transporter; BODIPY verapamil; Canalicular membrane; Cholesterol; HEK293 cell; Phosphatidylcholine; Phosphatidylethanolamine; Raft; Sphingomyelin; Triton X 100

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BILE SALT; CHOLESTEROL; FLOTILLIN 1; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 3; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; RHODAMINE 123; RHODAMINE 6G; SPHINGOMYELIN; TAUROCHOLIC ACID; TRANSFERRIN RECEPTOR; VERAPAMIL;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; LIPID ANALYSIS; LIPID COMPOSITION; LIPID RAFT; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NONRAFT MEMBRANE; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; BILE ACIDS AND SALTS; GENE EXPRESSION REGULATION; HEK293 CELLS; HEPATOCYTES; HUMANS; MEMBRANE MICRODOMAINS; MICE; P-GLYCOPROTEIN; P-GLYCOPROTEINS; PHOSPHOLIPIDS; RHODAMINE 123; RHODAMINES;

EID: 84876803699     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M032425     Document Type: Article

References (57)

1. Oude Elferink, R. P., and C. C. Paulusma. 2007. Function and pathophysiological importance of ABCB4 (MDR3 P-glycoprotein). Pfl ugers Arch. 453 : 601-610.
2. Borst, P., N. Zelcer, and A. van Helvoort. 2000. ABC transporters in lipid transport. Biochim. Biophys. Acta. 1486 : 128-144.
3. Smit, J. J., A. H. Schinkel, R. P. Oude Elferink, A. K. Groen, E. Wagenaar, L. van Deemter, C. A. Mol, R. Ottenhoff, N. M. van der Lugt, M. A. van Roon, et al. 1993. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell. 75 : 451-462.
4. Oude Elferink, R. P., R. Ottenhoff, M. van Wijland, C. M. Frijters, C. van Nieuwkerk, and A. K. Groen. 1996. Uncoupling of biliary phospholipid and cholesterol secretion in mice with reduced expression of mdr2 P-glycoprotein. J. Lipid Res. 37 : 1065-1075.
5. Smith, A. J., J. M. de Vree, R. Ottenhoff, R. P. Oude Elferink, A. H. Schinkel, and P. Borst. 1998. Hepatocyte-specific expression of the human MDR3 P-glycoprotein gene restores the biliary phosphatidylcholine excretion absent in Mdr2 (α /α) mice. Hepatology. 28 : 530-536.
6. Langheim, S., L. Yu, K. von Bergmann, D. Lutjohann, F. Xu, H. H. Hobbs, and J. C. Cohen. 2005. ABCG5 and ABCG8 require MDR2 for secretion of cholesterol into bile. J. Lipid Res. 46 : 1732-1738.
7. Deleuze, J. F., E. Jacquemin, C. Dubuisson, D. Cresteil, M. Dumont, S. Erlinger, O. Bernard, and M. Hadchouel. 1996. Defect of multidrug-resistance 3 gene expression in a subtype of progressive familial intrahepatic cholestasis. Hepatology. 23 : 904-908.
8. de Vree, J. M., E. Jacquemin, E. Sturm, D. Cresteil, P. J. Bosma, J. Aten, J. F. Deleuze, M. Desrochers, M. Burdelski, O. Bernard, et al. 1998. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc. Natl. Acad. Sci. USA. 95 : 282-287.
9. Lucena, J. F., J. I. Herrero, J. Quiroga, B. Sangro, J. Garcia-Foncillas, N. Zabalegui, J. Sola, M. Herraiz, J. F. Medina, and J. Prieto. 2003. A multidrug resistance 3 gene mutation causing cholelithiasis, cholestasis of pregnancy, and adulthood biliary cirrhosis. Gastroenterology. 124 : 1037-1042.
10. Oude Elferink, R. P., R. Ottenhoff, M. van Wijland, J. J. Smit, A. H. Schinkel, and A. K. Groen. 1995. Regulation of biliary lipid secretion by mdr2 P-glycoprotein in the mouse. J. Clin. Invest. 95 : 31-38.
11. Morita, S. Y., A. Kobayashi, Y. Takanezawa, N. Kioka, T. Handa, H. Arai, M. Matsuo, and K. Ueda. 2007. Bile salt-dependent efflux of cellular phospholipids mediated by ATP binding cassette protein B4. Hepatology. 46 : 188-199.
12. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: A physiological role for the mdr2 gene. Cell. 77 : 1071-1081.
13. Smith, A. J., J. L. Timmermans-Hereijgers, B. Roelofsen, K. W. Wirtz, W. J. van Blitterswijk, J. J. Smit, A. H. Schinkel, and P. Borst. 1994. The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fi broblasts from transgenic mice. FEBS Lett. 354 : 263-266.
14. van Helvoort, A., A. J. Smith, H. Sprong, I. Fritzsche, A. H. Schinkel, P. Borst, and G. van Meer. 1996. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifi-cally translocates phosphatidylcholine. Cell. 87 : 507-517.
15. Crawford, A. R., A. J. Smith, V. C. Hatch, R. P. Oude Elferink, P. Borst, and J. M. Crawford. 1997. Hepatic secretion of phospholipid vesicles in the mouse critically depends on mdr2 or MDR3 P-glycoprotein expression. Visualization by electron microscopy. J. Clin. Invest. 100 : 2562-2567.
16. Groen, A., M. R. Romero, C. Kunne, S. J. Hoosdally, P. H. Dixon, C. Wooding, C. Williamson, J. Seppen, K. Van den Oever, K. S. Mok, et al. 2011. Complementary functions of the fl ippase ATP8B1 and the fl oppase ABCB4 in maintaining canalicular membrane integrity. Gastroenterology. 141 : 1927-1937.
17. Ruetz, S., and P. Gros. 1995. Enhancement of Mdr2-mediated phosphatidylcholine translocation by the bile salt taurocholate. Implications for hepatic bile formation. J. Biol. Chem. 270 : 25388-25395.
18. Gottesman, M. M., T. Fojo, and S. E. Bates. 2002. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer. 2 : 48-58.
19. Schinkel, A. H., E. M. Roelofs, and P. Borst. 1991. Characterization of the human MDR3 P-glycoprotein and its recognition by P-glycoprotein-specific monoclonal antibodies. Cancer Res. 51 : 2628-2635.
20. Smith, A. J., A. van Helvoort, G. van Meer, K. Szabo, E. Welker, G. Szakacs, A. Varadi, B. Sarkadi, and P. Borst. 2000. MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly interacts with drugs as judged by interference with nucleotide trapping. J. Biol. Chem. 275 : 23530-23539.
21. Kino, K., Y. Taguchi, K. Yamada, T. Komano, and K. Ueda. 1996. Aureobasidin A, an antifungal cyclic depsipeptide antibiotic, is a substrate for both human MDR1 and MDR2/P-glycoproteins. FEBS Lett. 399 : 29-32.
22. Yoshikado, T., T. Takada, T. Yamamoto, H. Yamaji, K. Ito, T. Santa, H. Yokota, Y. Yatomi, H. Yoshida, J. Goto, et al. 2011. Itraconazoleinduced cholestasis: Involvement of the inhibition of bile canalicular phospholipid translocator MDR3/ABCB4. Mol. Pharmacol. 79 : 241-250.
23. Zhou, Y., M. M. Gottesman, and I. Pastan. 1999. Studies of human MDR1-MDR2 chimeras demonstrate the functional exchangeability of a major transmembrane segment of the multidrug transporter and phosphatidylcholine fl ippase. Mol. Cell. Biol. 19 : 1450-1459.
24. Zhou, Y., M. M. Gottesman, and I. Pastan. 1999. Domain exchangeability between the multidrug transporter (MDR1) and phosphatidylcholine fl ippase (MDR2). Mol. Pharmacol. 56 : 997-1004.
25. Orlowski, S., S. Martin, and A. Escargueil. 2006. P-glycoprotein and 'lipid rafts': Some ambiguous mutual relationships (fl oating on them, building them or meeting them by chance?). Cell. Mol. Life Sci. 63 : 1038-1059.
26. Klappe, K., I. Hummel, D. Hoekstra, and J. W. Kok. 2009. Lipid dependence of ABC transporter localization and function. Chem. Phys. Lipids. 161 : 57-64.
27. Quinn, P. J. 2010. A lipid matrix model of membrane raft structure. Prog. Lipid Res. 49 : 390-406.
28. Prpi, V., K. C. Green, P. F. Blackmore, and J. H. Exton. 1984. Vasopressin-, angiotensin II-, and alpha 1-adrenergic-induced inhibition of Ca2+ transport by rat liver plasma membrane vesicles. J. Biol. Chem. 259 : 1382-1385.
29. Kobayashi, K., Y. Sogame, H. Hara, and K. Hayashi. 1990. Mechanism of glutathione S-conjugate transport in canalicular and basolateral rat liver plasma membranes. J. Biol. Chem. 265 : 7737-7741.
30. Newman, E. A., S. J. Muh, R. H. Hovhannisyan, C. C. Warzecha, R. B. Jones, W. L. McKeehan, and R. P. Carstens. 2006. Identification of RNA-binding proteins that regulate FGFR2 splicing through the use of sensitive and specific dual color fl uorescence minigene assays. RNA. 12 : 1129-1141.
31. Zaks-Makhina, E., H. Li, A. Grishin, V. Salvador-Recatala, and E. S. Levitan. 2009. Specific and slow inhibition of the kir2.1 K+ channel by gambogic acid. J. Biol. Chem. 284 : 15432-15438.
32. Amundson, D. M., and M. Zhou. 1999. Fluorometric method for the enzymatic determination of cholesterol. J. Biochem. Biophys. Methods. 38 : 43-52.
33. Morita, S. Y., A. Takeuchi, and S. Kitagawa. 2010. Functional analysis of two isoforms of phosphatidylethanolamine N-methyltransferase. Biochem. J. 432 : 387-398.
34. Morita, S. Y., K. Soda, R. Teraoka, S. Kitagawa, and T. Terada. 2012. Specific and sensitive enzymatic measurement of sphingomyelin in cultured cells. Chem. Phys. Lipids. 165 : 571-576.
35. Macdonald, J. L., and L. J. Pike. 2005. A simplifi ed method for the preparation of detergent-free lipid rafts. J. Lipid Res. 46 : 1061-1067.
36. Abe-Dohmae, S., S. Suzuki, Y. Wada, H. Aburatani, D. E. Vance, and S. Yokoyama. 2000. Characterization of apolipoprotein-mediated HDL generation induced by cAMP in a murine macrophage cell line. Biochemistry. 39 : 11092-11099.
37. Georges, E., G. Bradley, J. Gariepy, and V. Ling. 1990. Detection of P-glycoprotein isoforms by gene-specific monoclonal antibodies. Proc. Natl. Acad. Sci. USA. 87 : 152-156.
38. Scheffer, G. L., M. Kool, M. Heijn, M. de Haas, A. C. Pijnenborg, J. Wijnholds, A. van Helvoort, M. C. de Jong, J. H. Hooijberg, C. A. Mol, et al. 2000. Specific detection of multidrug resistance proteins MRP1, MRP2, MRP3, MRP5, and MDR3 P-glycoprotein with a panel of monoclonal antibodies. Cancer Res. 60 : 5269-5277.
39. Nagao, K., K. Takahashi, K. Hanada, N. Kioka, M. Matsuo, and K. Ueda. 2007. Enhanced apoA-I-dependent cholesterol efflux by ABCA1 from sphingomyelin-deficient Chinese hamster ovary cells. J. Biol. Chem. 282 : 14868-14874.
40. Mendez, A. J., G. Lin, D. P. Wade, R. M. Lawn, and J. F. Oram. 2001. Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J. Biol. Chem. 276 : 3158-3166.
41. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68 : 533-544.
42. Romanenko, V. G., Y. Fang, F. Byfield, A. J. Travis, C. A. Vandenberg, G. H. Rothblat, and I. Levitan. 2004. Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels. Biophys. J. 87 : 3850-3861.
43. Meyer dos Santos, S., C. C. Weber, C. Franke, W. E. Muller, and G. P. Eckert. 2007. Cholesterol: Coupling between membrane microenvironment and ABC transporter activity. Biochem. Biophys. Res. Commun. 354 : 216-221. [Erratum. 2011. Biochem. Biophys. Res. Commun. 408: 193.]
44. Storch, C. H., R. Ehehalt, W. E. Haefeli, and J. Weiss. 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.
45. Troost, J., H. Lindenmaier, W. E. Haefeli, and J. Weiss. 2004. Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells. Mol. Pharmacol. 66 : 1332-1339.
46. Kimura, Y., N. Kioka, H. Kato, M. Matsuo, and K. Ueda. 2007. Modulation of drug-stimulated ATPase activity of human MDR1/Pglycoprotein by cholesterol. Biochem. J. 401 : 597-605.
47. Zastre, J. A., J. K. Jackson, W. Wong, and H. M. Burt. 2008. P-glycoprotein efflux inhibition by amphiphilic diblock copolymers: Relationship between copolymer concentration and substrate hydrophobicity. Mol. Pharm. 5 : 643-653.
48. Luker, G. D., C. M. Pica, A. S. Kumar, D. F. Covey, and D. Piwnica-Worms. 2000. Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry. 39 : 7651-7661.
49. Mazzanti, R., O. Fantappie, Y. Kamimoto, Z. Gatmaitan, P. Gentilini, and I. M. Arias. 1994. Bile acid inhibition of P-glycoproteinmediated transport in multidrug-resistant cells and rat liver canalicular membrane vesicles. Hepatology. 20 : 170-176.
50. Landry, Y. D., M. Denis, S. Nandi, S. Bell, A. M. Vaughan, and X. Zha. 2006. ATP-binding cassette transporter A1 expression disrupts raft membrane microdomains through its ATPase-related functions. J. Biol. Chem. 281 : 36091-36101.
51. Cerf, E., R. Gasper, J. D. Belani, S. Rychnovsky, X. B. Chang, F. Buyse, and J. M. Ruysschaert. 2007. Multidrug resistance protein 1 is not associated to detergent-resistant membranes. Biochem. Biophys. Res. Commun. 355 : 1025-1030. [Erratum. 2008. Biochem. Biophys. Res. Commun. 366: 605.]
52. Kremmer, T., M. H. Wisher, and W. H. Evans. 1976. The lipid composition of plasma membrane subfractions originating from the three major functional domains of the rat hepatocyte cell surface. Biochim. Biophys. Acta. 455 : 655-664.
53. Eckhardt, E. R., A. Moschetta, W. Renooij, S. S. Goerdayal, G. P. van Berge-Henegouwen, and K. J. van Erpecum. 1999. Asymmetric distribution of phosphatidylcholine and sphingomyelin between micellar and vesicular phases. Potential implications for canalicular bile formation. J. Lipid Res. 40 : 2022-2033.
54. Alvaro, D., A. Cantafora, A. F. Attili, S. Ginanni Corradini, C. De Luca, G. Minervini, A. Di Biase, and M. Angelico. 1986. Relationships between bile salts hydrophilicity and phospholipid composition in bile of various animal species. Comp. Biochem. Physiol. B. 83 : 551-554.
55. Vance, J. E. 2008. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: Two metabolically related aminophospholipids. J. Lipid Res. 49 : 1377-1387.
56. Pennings, M., R. B. Hildebrand, D. Ye, C. Kunne, T. J. Van Berkel, A. K. Groen, and M. Van Eck. 2007. Bone marrow-derived multidrug resistance protein ABCB4 protects against atherosclerotic lesion development in LDL receptor knockout mice. Cardiovasc. Res. 76 : 175-183.
57. Nagao, K., Y. Zhao, K. Takahashi, Y. Kimura, and K. Ueda. 2009. Sodium taurocholate-dependent lipid efflux by ABCA1: Effects of W590S mutation on lipid translocation and apolipoprotein A-I dissociation. J. Lipid Res. 50 : 1165-1172.