P-glycoprotein dysfunction contributes to hepatic steatosis and obesity in mice

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Foucaud Vignault, Magali ^a   Soayfane, Zeina ^a,b,c   Ménez, Cécile ^a   Bertrand Michel, Justine ^d   Martin, Pascal Guy Pierre ^a   Guillou, Hervé ^a   Collet, Xavier ^b,c   Lespine, Anne ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b CNRS   (France)

^c University Hospital of Toulouse   (France)

^d IFR150   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLYCOPROTEIN P; INSULIN; TRIACYLGLYCEROL; ACYL COENZYME A DESATURASE; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; CYP2B10 PROTEIN, MOUSE; FATTY ACID SYNTHASE; LIPID; MULTIDRUG RESISTANCE PROTEIN 3; P GLYCOPROTEIN 2; P-GLYCOPROTEIN 2; SCD1 PROTEIN, MOUSE; STEROID MONOOXYGENASE; UNSPECIFIC MONOOXYGENASE;

ACOX GENE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD36 GENE; CONTROLLED STUDY; CYP2B10 GENE; CYP3A11 GENE; FASN GENE; FATTY LIVER; FEMALE; FOOD INTAKE; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYPERTROPHY; IN VIVO STUDY; INSULIN BLOOD LEVEL; LIPID COMPOSITION; LIPID DIET; LIPID METABOLISM; LIPOGENESIS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; ORGAN WEIGHT; SCD 1 GENE; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BLOOD; BODY WEIGHT; EATING; GENETICS; LIVER; METABOLISM; MOUSE MUTANT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHITE ADIPOSE TISSUE;

MUS;

ADIPOSE TISSUE, WHITE; ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BLOOD GLUCOSE; BODY WEIGHT; DIET, HIGH-FAT; EATING; FATTY ACID SYNTHETASE COMPLEX; FATTY LIVER; FEMALE; GENE EXPRESSION; INSULIN; LIPIDS; LIVER; MALE; MICE; MICE, KNOCKOUT; OBESITY; P-GLYCOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEAROYL-COA DESATURASE; STEROID HYDROXYLASES;

EID: 80052869641     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023614     Document Type: Article

References (49)

1. Juliano RL, Ling V, (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 455: 152-162.
2. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, et al. (1987) Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci U S A 84: 7735-7738.
3. Schinkel AH, Jonker JW, (2003) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55: 3-29.
4. Kwei GY, Alvaro RF, Chen Q, Jenkins HJ, Hop CE, et al. (1999) Disposition of ivermectin and cyclosporin A in CF-1 mice deficient in mdr1a P-glycoprotein. Drug Metab Dispos 27: 581-587.
5. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Deemter L, et al. (1997) Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci U S A 94: 4028-4033.
6. Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, et al. (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77: 491-502.
7. Schinkel AH, Wagenaar E, van Deemter L, Mol CA, Borst P, (1995) Absence of the mdr1a P-Glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporin A. J Clin Invest 96: 1698-1705.
8. Honig SM, Fu S, Mao X, Yopp A, Gunn MD, et al. (2003) FTY720 stimulates multidrug transporter- and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J Clin Invest 111: 627-637.
9. Aye IL, Singh AT, Keelan JA, (2009) Transport of lipids by ABC proteins: interactions and implications for cellular toxicity, viability and function. Chem Biol Interact 180: 327-339.
10. Tessner TG, Stenson WF, (2000) Overexpression of MDR1 in an intestinal cell line results in increased cholesterol uptake from micelles. Biochem Biophys Res Commun 267: 565-571.
11. Garrigues A, Escargueil AE, Orlowski S, (2002) The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci U S A 99: 10347-10352.
12. Gayet L, Dayan G, Barakat S, Labialle S, Michaud M, et al. (2005) Control of P-glycoprotein activity by membrane cholesterol amounts and their relation to multidrug resistance in human CEM leukemia cells. Biochemistry 44: 4499-4509.
13. Rothnie A, Theron D, Soceneantu L, Martin C, Traikia M, et al. (2001) The importance of cholesterol in maintenance of P-glycoprotein activity and its membrane perturbing influence. Eur Biophys J 30: 430-442.
14. Luker GD, Nilsson KR, Covey DF, Piwnica-Worms D, (1999) Multidrug resistance (MDR1) P-glycoprotein enhances esterification of plasma membrane cholesterol. J Biol Chem 274: 6979-6991.
15. Hu CC, Qing K, Chen Y, (2004) Diet-induced changes in stearoyl-CoA desaturase 1 expression in obesity-prone and-resistant mice. Obes Res 12: 1264-1270.
16. Jeannesson E, Siest G, Bastien B, Albertini L, Aslanidis C, et al. (2009) Association of ABCB1 gene polymorphisms with plasma lipid and apolipoprotein concentrations in the STANISLAS cohort. Clin Chim Acta 403: 198-202.
17. Kajinami K, Brousseau ME, Ordovas JM, Schaefer EJ, (2004) Polymorphisms in the multidrug resistance-1 (MDR1) gene influence the response to atorvastatin treatment in a gender-specific manner. Am J Cardiol 93: 1046-1050.
18. Rodrigues AC, Rebecchi IM, Bertolami MC, Faludi AA, Hirata MH, et al. (2005) High baseline serum total and LDL cholesterol levels are associated with MDR1 haplotypes in Brazilian hypercholesterolemic individuals of European descent. Braz J Med Biol Res 38: 1389-1397.
19. Ichihara S, Yamada Y, Kato K, Hibino T, Yokoi K, et al. (2008) Association of a polymorphism of ABCB1 with obesity in Japanese individuals. Genomics 91: 512-516.
20. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
21. Vieu C, Jaspard B, Barbaras R, Manent J, Chap H, et al. (1996) Identification and quantification of diacylglycerols in HDL and accessibility to lipase. J Lipid Res 37: 1153-1161.
22. Batt RA, Wilson CA, Topping DL, (1978) Potentiation of hyperphagia and relief of hypothermia in the genetically obese mouse (genotype, ob/ob) by alpha-methyl tyrosine. Int J Obes 2: 303-307.
23. Cox JE, Powley TL, (1977) Development of obesity in diabetic mice pair-fed with lean siblings. J Comp Physiol Psychol 91: 347-358.
24. Yanase T, Fan W, Kyoya K, Min L, Takayanagi R, et al. (2008) Androgens and metabolic syndrome: lessons from androgen receptor knock out (ARKO) mice. J Steroid Biochem Mol Biol 109: 254-257.
25. Ntambi JM, Miyazaki M, Stoehr JP, Lan H, Kendziorski CM, et al. (2002) Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc Natl Acad Sci U S A 99: 11482-11486.
26. Haluzik M, Colombo C, Gavrilova O, Chua S, Wolf N, et al. (2004) Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology 145: 3258-3264.
27. Coburn CT, Knapp FF Jr, Febbraio M, Beets AL, Silverstein RL, et al. (2000) Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem 275: 32523-32529.
28. Terpstra V, van Amersfoort ES, van Velzen AG, Kuiper J, van Berkel TJ, (2000) Hepatic and extrahepatic scavenger receptors: function in relation to disease. Arterioscler Thromb Vasc Biol 20: 1860-1872.
29. Le Lay S, Boucher J, Rey A, Castan-Laurell I, Krief S, et al. (2001) Decreased resistin expression in mice with different sensitivities to a high-fat diet. Biochem Biophys Res Commun 289: 564-567.
30. Rogue A, Spire C, Brun M, Claude N, Guillouzo A, (2010) Gene Expression Changes Induced by PPAR Gamma Agonists in Animal and Human Liver. PPAR Res 2010.
31. Ducheix S, Lobaccaro JM, Martin PG, Guillou H, (2011) Liver X Receptor: an oxysterol sensor and a major player in the control of lipogenesis. Chem Phys Lipids 164: 500-514.
32. Chiang JY, Kimmel R, Stroup D, (2001) Regulation of cholesterol 7alpha-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRalpha). Gene 262: 257-265.
33. Cao G, Beyer TP, Yang XP, Schmidt RJ, Zhang Y, et al. (2002) Phospholipid transfer protein is regulated by liver X receptors in vivo. J Biol Chem 277: 39561-39565.
34. Thornton SJ, Wong E, Lee SD, Wasan KM, (2008) Effect of dietary fat on hepatic liver X receptor expression in P-glycoprotein deficient mice: implications for cholesterol metabolism. Lipids Health Dis 7: 21.
35. Kohle C, Bock KW, (2009) Coordinate regulation of human drug-metabolizing enzymes, and conjugate transporters by the Ah receptor, pregnane X receptor and constitutive androstane receptor. Biochem Pharmacol 77: 689-699.
36. Moore LB, Maglich JM, McKee DD, Wisely B, Willson TM, et al. (2002) Pregnane X receptor (PXR), constitutive androstane receptor (CAR), and benzoate X receptor (BXR) define three pharmacologically distinct classes of nuclear receptors. Mol Endocrinol 16: 977-986.
37. Casabar RC, Das PC, Dekrey GK, Gardiner CS, Cao Y, et al. (2010) Endosulfan induces CYP2B6 and CYP3A4 by activating the pregnane X receptor. Toxicol Appl Pharmacol 245: 335-343.
38. Conseil G, Baubichon-Cortay H, Dayan G, Jault JM, Barron D, et al. (1998) Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc Natl Acad Sci U S A 95: 9831-9836.
39. Wang H, Li H, Moore LB, Johnson MD, Maglich JM, et al. (2008) The phytoestrogen coumestrol is a naturally occurring antagonist of the human pregnane X receptor. Mol Endocrinol 22: 838-857.
40. Schuetz EG, Umbenhauer DR, Yasuda K, Brimer C, Nguyen L, et al. (2000) Altered expression of hepatic cytochromes P-450 in mice deficient in one or more mdr1 genes. Mol Pharmacol 57: 188-197.
41. Maglich JM, Lobe DC, Moore JT, (2009) The nuclear receptor CAR (NR1I3) regulates serum triglyceride levels under conditions of metabolic stress. J Lipid Res 50: 439-445.
42. Zhou J, Zhai Y, Mu Y, Gong H, Uppal H, et al. (2006) A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. J Biol Chem 281: 15013-15020.
43. Breuker C, Moreau A, Lakhal L, Tamasi V, Parmentier Y, et al. (2010) Hepatic expression of thyroid hormone-responsive spot 14 protein is regulated by constitutive androstane receptor (NR1I3). Endocrinology 151: 1653-1661.
44. Hoffmeyer S, Burk O, von Richter O, Arnold HP, Brockmoller J, et al. (2000) Functional polymorphisms of the human multidrug-resistance gene: multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci U S A 97: 3473-3478.
45. Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM, (2007) Silent polymorphisms speak: how they affect pharmacogenomics and the treatment of cancer. Cancer Res 67: 9609-9612.
46. Giralt M, Diaz-Delfin J, Gallego-Escuredo JM, Villarroya J, Domingo P, et al. (2010) Lipotoxicity on the basis of metabolic syndrome and lipodystrophy in HIV-1-infected patients under antiretroviral treatment. Curr Pharm Des 16: 3371-3378.
47. Okura T, Ibe M, Umegaki K, Shinozuka K, Yamada S, (2010) Effects of dietary ingredients on function and expression of P-glycoprotein in human intestinal epithelial cells. Biol Pharm Bull 33: 255-259.
48. Mealey KL, Bentjen SA, Gay JM, Cantor GH, (2001) Ivermectin sensitivity in collies is associated with a deletion mutation of the mdr1 gene. Pharmacogenetics 11: 727-733.
49. Roulet A, Puel O, Gesta S, Lepage JF, Drag M, et al. (2003) MDR1-deficient genotype in Collie dogs hypersensitive to the P-glycoprotein substrate ivermectin. Eur J Pharmacol 460: 85-91.