The hepatic phosphatidylcholine transporter ABCB4 as modulator of glucose homeostasis

FASEB Journal

Volumn 26, Issue 12, 2012, Pages 5081-5091

  Hochrath, Katrin ^a   Krawczyk, Marcin ^a   Goebel, Reinhild ^a   Langhirt, Miriam ^a   Rathkolb, Birgit ^b,c   Micklich, Kateryna ^b,c   Rozman, Jan ^c,d   Horsch, Marion ^b   Beckers, Johannes ^c,d   Klingenspor, Martin ^d   Fuchs, Helmut ^c   Gailus Durner, Valérie ^c   Wolf, Eckhard ^b   Acalovschi, Monica ^e   Volmer, Dietrich A ^f   De Angelis, Martin Hrabě ^c,e,g   Lammert, Frank ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e IULIU HATIEGANU UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^f SAARLAND UNIVERSITY   (Germany)

^g GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

ATP binding cassette transporter; Chronic cholangitis; Liver fibrosis; Liver receptor homolog

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER B4; GLUCOSE; LIVER RECEPTOR HOMOLOG 1; RNA; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE EXPRESSION; GENETIC VARIABILITY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HUMAN; LIVER HISTOLOGY; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; COHORT STUDIES; FEMALE; GALLSTONES; GENE EXPRESSION PROFILING; HOMEOSTASIS; HUMANS; LIVER; MALE; MICE; MICE, CONGENIC; MICE, INBRED BALB C; MICE, KNOCKOUT; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; P-GLYCOPROTEINS; PHOSPHATIDYLCHOLINES; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; YOUNG ADULT;

MUS;

EID: 84870330834     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-209379     Document Type: Article

References (55)

1. Carey, M. C., and LaMont, J. T. (1992) Cholesterol gallstone formation. 1. Physical-chemistry of bile and biliary lipid secretion. Prog. Liver Dis. 10, 139-163
2. Oude Elferink, R. P., Paulusma, C. C., and Groen, A. K. (2006) Hepatocanalicular transport defects: pathophysiologic mechanisms of rare diseases. Gastroenterology 130, 908-925 (Pubitemid 43374538)
3. Krawczyk, M., Wang, D. Q., Portincasa, P., and Lammert, F. (2011) Dissecting the genetic heterogeneity of gallbladder stone formation. Semin. Liver Dis. 31, 157-172
4. Müllenbach, R., Linton, K. J., Wiltshire, S., Weerasekera, N., Chambers, J., Elias, E., Higgins, C. F., Johnston, D. G., McCarthy, M. I., and Williamson, C. (2003) ABCB4 gene sequence variation in women with intrahepatic cholestasis of pregnancy. J. Med. Genet. 40, e70
5. Wasmuth, H. E., Glantz, A., Keppeler, H., Simon, E., Bartz, C., Rath, W., Mattsson, L. A., Marschall, H. U., and Lammert, F. (2007) Intrahepatic cholestasis of pregnancy: the severe form is associated with common variants of the hepatobiliary phospholipid transporter ABCB4 gene. Gut 56, 265-270
6. Rosmorduc, O., Hermelin, B., and Poupon, R. (2001) MDR3 gene defect in adults with symptomatic intrahepatic and gallbladder cholesterol cholelithiasis. Gastroenterology 120, 1459-1467 (Pubitemid 32322320)
7. Rosmorduc, O., Hermelin, B., Boelle, P. Y., Parc, R., Taboury, J., and Poupon, R. (2003) ABCB4 gene mutation-associated cholelithiasis in adults. Gastroenterology 125, 452-459 (Pubitemid 36929427)
8. Smit, J. J., Schinkel, A. H., Oude Elferink, R. P., Groen, A. K., Wagenaar, E., van Deemter, L., Mol, C. A., Ottenhoff, R., van der Lugt, N. M., and van Roon, M. A. (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 (Pubitemid 23335071)
9. -/- mice: a model for low phospholipid-associated cholelithiasis. Hepatology 39, 117-128
10. Fickert, P., Fuchsbichler, A., Wagner, M., Zollner, G., Kaser, A., Tilg, H., Krause, R., Lammert, F., Langner, C., Zatloukal, K., Marschall, H. U., Denk, H., and Trauner, M. (2004) Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 127, 261-274 (Pubitemid 38962293)
11. Vacca, M., Krawczyk, M., Petruzzelli, M., Sasso, R. C., van Erpecum, K. J., Palasciano, G., van Berge-Henegouwen, G. P., Moschetta, A., and Portincasa, P. (2007) Current treatments of primary sclerosing cholangitis. Curr. Med. Chem. 14, 2081-2094 (Pubitemid 47578165)
12. Forman, B. M. (2005) Are those phospholipids in your pocket? Cell Metab. 1, 153-155
13. Lee, J. M., Lee, Y. K., Mamrosh, J. L., Busby, S. A., Griffin, P. R., Pathak, M. C., Ortlund, E. A., and Moore, D. D. (2011) A nuclear-receptor- dependent phosphatidylcholine pathway with antidiabetic effects. Nature 474, 506-510
14. Fayard, E., Auwerx, J., and Schoonjans, K. (2004) LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol. 14, 250-260 (Pubitemid 38591329)
15. Roderick, S. L., Chan, W. W., Agate, D. S., Olsen, L. R., Vetting, M. W., Rajashankar, K. R., and Cohen, D. E. (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat. Struct. Biol. 9, 507-511 (Pubitemid 34693804)
16. Shishova, E. Y., Stoll, J. M., Ersoy, B. A., Shrestha, S., Scapa, E. F., Li, Y., Niepel, M. W., Su, Y., Jelicks, L. A., Stahl, G. L., Glicksman, M. A., Gutierrez-Juarez, R., Cuny, G. D., and Cohen, D. E. (2011) Genetic ablation or chemical inhibition of phosphatidylcholine transfer protein attenuates diet-induced hepatic glucose production. Hepatology 54, 664-674
17. -/- mice spontaneously develop severe biliary fibrosis via massive dysregulation of pro- and antifibrogenic genes. J. Hepatol. 43, 1045-1054
18. Iyengar, S. K., Abboud, H. E., Goddard, K. A., Saad, M. F., Adler, S. G., Arar, N. H., Bowden, D. W., Duggirala, R., Elston, R. C., Hanson, R. L., Ipp, E., Kao, W. H., Kimmel, P. L., Klag, M. J., Knowler, W. C., Meoni, L. A., Nelson, R. G., Nicholas, S. B., Pahl, M. V., Parekh, R. S., Quade, S. R., Rich, S. S., Rotter, J. I., Scavini, M., Schelling, J. R., Sedor, J. R., Sehgal, A. R., Shah, V. O., Smith, M. W., Taylor, K. D., Winkler, C. A., Zager, P. G., and Freedman, B. I. (2007) Genome-wide scans for diabetic nephropathy and albuminuria in multiethnic populations: the family investigation of nephropathy and diabetes (FIND). Diabetes 56, 1577-1585 (Pubitemid 46842614)
19. Prochazka, M., Mochizuki, H., Baier, L. J., Cohen, P. T., and Bogardus, C. (1995) Molecular and linkage analysis of type-1 protein phosphatase catalytic beta-subunit gene: lack of evidence for its major role in insulin resistance in Pima Indians. Diabetologia 38, 461-466
20. Mochizuki, H., Scherer, S. W., Xi, T., Nickle, D. C., Majer, M., Huizenga, J. J., Tsui, L. C., and Prochazka, M. (1998) Human PON2 gene at 7q21.3: cloning, multiple mRNA forms, and missense polymorphisms in the coding sequence. Gene 213, 149-157 (Pubitemid 28284734)
21. Gailus-Durner, V., Fuchs, H., Becker, L., Bolle, I., Brielmeier, M., Calzada-Wack, J., Elvert, R., Ehrhardt, N., Dalke, C., Franz, T. J., Grundner-Culemann, E., Hammelbacher, S., Hölter, S. M., Hölzlwimmer, G., Horsch, M., Javaheri, A., Kalaydjiev, S. V., Klempt, M., Kling, E., Kunder, S., Lengger, C., Lisse, T., Mijalski, T., Naton, B., Pedersen, V., Prehn, C., Przemeck, G., Racz, I., Reinhard, C., Reitmeir, P., Schneider, I., Schrewe, A., Steinkamp, R., Zybill, C., Adamski, J., Beckers, J., Behrendt, H., Favor, J., Graw, J., Heldmaier, G., Höfler, H., Ivandic, B., Katus, H., Kirchhof, P., Klingenspor, M., Klopstock, T., Lengeling, A., Muller, W., Ohl, F., Ollert, M., Quintanilla-Martinez, L., Schmidt, J., Schulz, H., Wolf, E., Wurst, W., Zimmer, A., Busch, D. H., and Hrabe? de Angelis, M. (2005) Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat. Methods 2, 403-404 (Pubitemid 40916545)
22. Hillebrandt, S., Goos, C., Matern, S., and Lammert, F. (2002) Genome-wide analysis of hepatic fibrosis in inbred mice identifies the susceptibility locus Hfib1 on chromosome 15. Gastroenterology 123, 2041-2051 (Pubitemid 35408326)
23. Hillebrandt, S., Wasmuth, H. E., Weiskirchen, R., Hellerbrand, C., Keppeler, H., Werth, A., Schirin-Sokhan, R., Wilkens, G., Geier, A., Lorenzen, J., Kohl, J., Gressner, A. M., Matern, S., and Lammert, F. (2005) Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nat. Genet. 37, 835-843 (Pubitemid 41077109)
24. Jamall, I. S., Finelli, V. N., and Que Hee, S. S. (1981) A simple method to determine nanogram levels of 4-hdydroxyproline in biological tissues. Anal. Biochem. 112, 70-75
25. Hegde, P., Qi, R., Abernathy, K., Gay, C., Dharap, S., Gaspard, R., Hughes, J. E., Snesrud, E., Lee, N., and Quackenbush, J. (2000) A concise guide to cDNA microarray analysis. BioTechniques 29, 548-550, 552-544
26. Horsch, M., Schädler, S., Gailus-Durner, V., Fuchs, H., Meyer, H., Hrabě de Angelis, M., and Beckers, J. (2008) Systematic gene expression profiling of mouse model series reveals coexpressed genes. Proteomics 8, 1248-1256 (Pubitemid 351462930)
27. Quackenbush, J. (2002) Microarray data normalization and transformation. Nat. Genet. 32(Suppl.), 496-501
28. Tusher, V. G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98, 5116-5121 (Pubitemid 32397092)
29. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408 (Pubitemid 34164012)
30. Dooley, S., Hamzavi, J., Ciuclan, L., Godoy, P., Ilkavets, I., Ehnert, S., Ueberham, E., Gebhardt, R., Kanzler, S., Geier, A., Breitkopf, K., Weng, H., and Mertens, P. R. (2008) Hepatocyte-specific Smad7 expression attenuates TGF-β-mediated fibrogenesis and protects against liver damage. Gastroenterology 135, 642-659
31. Kovacs, P., Kress, R., Rocha, J., Kurtz, U., Miquel, J. F., Nervi, F., Méndez-Sánchez, N., Uribe, M., Bock, H. H., Schirin-Sokhan, R., Stumvoll, M., Mössner, J., Lammert, F., and Wittenburg, H. (2008) Variation of the gene encoding the nuclear bile salt receptor FXR and gallstone susceptibility in mice and humans. J. Hepatol. 48, 116-124 (Pubitemid 350191984)
32. Grünhage, F., Acalovschi, M., Tirziu, S., Walier, M., Wienker, T. F., Ciocan, A., Mosteanu, O., Sauerbruch, T., and Lammert, F. (2007) Increased gallstone risk in humans conferred by common variant of hepatic ATP-binding cassette transporter for cholesterol. Hepatology 46, 793-801 (Pubitemid 47436126)
33. Krawczyk, M., Rusticeanu, M., Grünhage, F., Mahler, M., Portincasa, P., Acalovschi, M., and Lammert, F. (2010) Analysis of the common vasoactive intestinal peptide receptor 1 polymorphism in gallstone patients. J. Gastrointestin. Liver Dis. 19, 273-277
34. Krawczyk, M., Grünhage, F., Mahler, M., Tirziu, S., Acalovschi, M., and Lammert, F. (2011) The common adiponutrin variant p.I148M does not confer gallstone risk but affects fasting glucose and triglyceride levels. J. Physiol. Pharmacol. 62, 369-375
35. Moles, A., Tarrats, N., Fernandez-Checa, J. C., and Mari, M. (2011) Cathepsin B overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann Pick disease. J. Biol. Chem. 287, 1178-1188
36. 4-induced rat cirrhosis. Int. J. Biochem. Cell Biol. 42, 287-296
37. Baghy, K., Dezso, K., Laszlo, V., Fullar, A., Peterfia, B., Paku, S., Nagy, P., Schaff, Z., Iozzo, R. V., and Kovalszky, I. (2011) Ablation of the decorin gene enhances experimental hepatic fibrosis and impairs hepatic healing in mice. Lab. Invest. 91, 439-451
38. Varela-Rey, M., Martinez-Lopez, N., Fernandez-Ramos, D., Embade, N., Calvisi, D. F., Woodhoo, A., Rodriguez, J., Fraga, M. F., Julve, J., Rodriguez-Millan, E., Frades, I., Torres, L., Luka, Z., Wagner, C., Esteller, M., Lu, S. C., Martinez-Chantar, M. L., and Mato, J. M. (2010) Fatty liver and fibrosis in glycine N-methyltransferase knockout mice is prevented by nicotinamide. Hepatology 52, 105-114
39. Borkham-Kamphorst, E., Drews, F., and Weiskirchen, R. (2011) Induction of lipocalin-2 expression in acute and chronic experimental liver injury moderated by pro-inflammatory cytokines interleukin-1β through nuclear factor-κB activation. Liver Int. 31, 656-665
40. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131 (Pubitemid 34496588)
41. Müllenbach, R., Weber, N. S., and Lammert, F. (2011) Nuclear receptor variants in liver disease. J. Lipids 2012, ID934707
42. Biddinger, S. B., Haas, J. T., Yu, B. B., Bezy, O., Jing, E., Zhang, W., Unterman, T. G., Carey, M. C., and Kahn, C. R. (2008) Hepatic insulin resistance directly promotes formation of cholesterol gallstones. Nat. Med. 14, 778-782
43. Scapa, E. F., Pocai, A., Wu, M. K., Gutierrez-Juarez, R., Glenz, L., Kanno, K., Li, H., Biddinger, S., Jelicks, L. A., Rossetti, L., and Cohen, D. E. (2008) Regulation of energy substrate utilization and hepatic insulin sensitivity by phosphatidylcholine transfer protein/StarD2. FASEB J. 22, 2579-2590 (Pubitemid 351948675)
44. Wopereis, S., Radonjic, M., Rubingh, C., van Erk, M., Smilde, A., van Duyvenvoorde, W., Cnubben, N., Kooistra, T., van Ommen, B., and Kleemann, R. (2012) Identification of prognostic and diagnostic biomarkers of glucose intolerance in ApoE3Leiden mice. Physiol. Genomics 44, 293-304
45. Ortlund, E. A., Lee, Y., Solomon, I. H., Hager, J. M., Safi, R., Choi, Y., Guan, Z., Tripathy, A., Raetz, C. R., McDonnell, D. P., Moore, D. D., and Redinbo, M. R. (2005) Modulation of human nuclear receptor LRH-1 activity by phospholipids and SHP. Nat. Struct. Mol. Biol. 12, 357-363 (Pubitemid 43093091)
46. Baghdasaryan, A., Fickert, P., Fuchsbichler, A., Silbert, D., Gumhold, J., Horl, G., Langner, C., Moustafa, T., Halilbasic, E., Claudel, T., and Trauner, M. (2008) Role of hepatic phospholipids in development of liver injury in Mdr2 (Abcb4) knockout mice. Liver Int. 28, 948-958 (Pubitemid 352044443)
47. Oosterveer, M. H., Mataki, C., Yamamoto, H., Harach, T., Moullan, N., van Dijk, T. H., Ayuso, E., Bosch, F., Postic, C., Groen, A. K., Auwerx, J., and Schoonjans, K. (2012) LRH-1-dependent glucose sensing determines intermediary metabolism in liver. J. Clin. Invest. 122, 2817-2826
48. Lee, Y. K., Schmidt, D. R., Cummins, C. L., Choi, M., Peng, L., Zhang, Y., Goodwin, B., Hammer, R. E., Mangelsdorf, D. J., and Kliewer, S. A. (2008) Liver receptor homolog-1 regulates bile acid homeostasis but is not essential for feedback regulation of bile acid synthesis. Mol. Endocrinol. 22, 1345-1356 (Pubitemid 351786995)
49. Keitel, V. (2012) Bile acids as extrahepatic and interorgan signaling molecules. In Hepatobiliary Transport in Health and Disease (Häussinger, D., Keitel, V., and Kubitz, R., eds) pp. 117-129, De Gruyter, Berlin
50. Watanabe, M., Houten, S. M., Mataki, C., Christoffolete, M. A., Kim, B. W., Sato, H., Messaddeq, N., Harney, J. W., Ezaki, O., Kodama, T., Schoonjans, K., Bianco, A. C., and Auwerx, J. (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439, 484-489 (Pubitemid 43152840)
51. Acalovschi, M., Tirziu, S., Chiorean, E., Krawczyk, M., Grünhage, F., and Lammert, F. (2009) Common variants of ABCB4 and ABCB11 and plasma lipid levels: a study in sib pairs with gallstones, and controls. Lipids 44, 521-526
52. De Vree, J. M., Jacquemin, E., Sturm, E., Cresteil, D., Bosma, P. J., Aten, J., Deleuze, J. F., Desrochers, M., Burdelski, M., Bernard, O., Oude Elferink, R. P., and Hadchouel, M. (1998) Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc. Natl. Acad. Sci. U. S. A. 95, 282-287 (Pubitemid 28103945)
53. Jung, C., Driancourt, C., Baussan, C., Zater, M., Hadchouel, M., Meunier-Rotival, M., Guiochon-Mantel, A., and Jacquemin, E. (2007) Prenatal molecular diagnosis of inherited cholestatic diseases. J. Pediatr. Gastroenterol. Nutr. 44, 453-458 (Pubitemid 46573228)
54. Lang, C., Meier, Y., Stieger, B., Beuers, U., Lang, T., Kerb, R., Kullak-Ublick, G. A., Meier, P. J., and Pauli-Magnus, C. (2007) Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug-induced liver injury. Pharmacogenet. Genomics 17, 47-60 (Pubitemid 46183791)
55. Hohenester, S., and Beuers, U. (2011) Phosphatidylcholines as regulators of glucose and lipid homeostasis: promises and potential risks. Hepatology 54, 2266-2268