Farnesoid X receptor inhibits the transcriptional activity of carbohydrate response element binding protein in human hepatocytes

Molecular and Cellular Biology

Volumn 33, Issue 11, 2013, Pages 2202-2211

  Caron, Sandrine ^a,b,c   Samanez, Carolina Huaman ^a,b,c   Dehondt, Hélène ^a,b,c   Ploton, Maheul ^a,b,c   Briand, Olivier ^a,b,c   Lien, Fleur ^a,b,c   Dorchies, Emilie ^a,b,c   Dumont, Julie ^a,b,c   Postic, Catherine ^d   Cariou, Bertrand ^e   Lefebvre, Philippe ^a,b,c   Staels, Bart ^a,b,c  

^a UNIV LILLE   (France)

^b INSERM   (France)

^c INSTITUT PASTEUR DE LILLE   (France)

^d INSTITUT COCHIN   (France)

^e L INSTITUT DU THORAX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN C3; BINDING PROTEIN; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN; FARNESOID X RECEPTOR; GLUCOSE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HISTONE H3; PYRUVATE KINASE; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CARBOHYDRATE DIET; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; DELETION MUTANT; EXPRESSION VECTOR; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BINDING SITES; CELL LINE; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOLYSIS; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTES; HISTONES; HUMANS; LIVER; LYSINE; MICE; NUCLEAR RECEPTOR CO-REPRESSOR 2; P300-CBP TRANSCRIPTION FACTORS; PEPTIDE FRAGMENTS; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; PYRUVATE KINASE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIALOGLYCOPROTEINS;

EID: 84878972563     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01004-12     Document Type: Article

References (50)

1. Bouché C, Serdy S, Kahn CR, Goldfine AB. 2004. The cellular fate of glucose and its relevance in type 2 diabetes. Endocr. Rev. 25:807-830.
2. Nordlie RC, Foster JD, Lange AJ. 1999. Regulation of glucose production by the liver. Annu. Rev. Nutr. 19:379-406.
3. Girard J, Ferré P, Foufelle F. 1997. Mechanisms by which carbohydrates regulate expression of genes for glycolytic and lipogenic enzymes. Annu. Rev. Nutr. 17:325-352.
4. de Luis O, Valero MC, Jurado LA. 2000. WBSCR14, a putative transcription factor gene deleted in Williams-Beuren syndrome: complete characterisation of the human gene and the mouse ortholog. Eur. J. Hum. Genet. 8:215-222.
5. Yamashita H, Takenoshita M, Sakurai M, Bruick RK, Henzel WJ, Shillinglaw W, Arnot D, Uyeda K. 2001. A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc. Natl. Acad. Sci. U. S. A. 98:9116-9121.
6. Ma L, Tsatsos NG, Towle HC. 2005. Direct role of ChREBP. Mlx in regulating hepatic glucose-responsive genes. J. Biol. Chem. 280:12019-12027.
7. Iizuka K, Bruick RK, Liang G, Horton JD, Uyeda K. 2004. Deficiency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis. Proc. Natl. Acad. Sci. U. S. A. 101:7281-7286.
8. Ishii S, Iizuka K, Miller BC, Uyeda K. 2004. Carbohydrate response element binding protein directly promotes lipogenic enzyme gene transcription. Proc. Natl. Acad. Sci. U. S. A. 101:15597-15602.
9. Kawaguchi T, Takenoshita M, Kabashima T, Uyeda K. 2001. Glucose and cAMP regulate the L-type pyruvate kinase gene by phosphorylation/ dephosphorylation of the carbohydrate response element binding protein. Proc. Natl. Acad. Sci. U. S. A. 98:13710-13715.
10. Kabashima T, Kawaguchi T, Wadzinski BE, Uyeda K. 2003. Xylulose 5-phosphate mediates glucose-induced lipogenesis by xylulose 5-phosphate- activated protein phosphatase in rat liver. Proc. Natl. Acad. Sci. U. S. A. 100:5107-5112.
11. Dentin R, Tomas-Cobos L, Foufelle F, Leopold J, Girard J, Postic C, Ferré P. 2012. Glucose 6-phosphate, rather than xylulose 5-phosphate, is required for the activation of ChREBP in response to glucose in the liver. J. Hepatol. 56:199-209.
12. Li MV, Chen W, Harmancey RN, Nuotio-Antar AM, Imamura M, Saha P, Taegtmeyer H, Chan L. 2010. Glucose-6-phosphate mediates activa- tion of the carbohydrate responsive binding protein (ChREBP). Biochem. Biophys. Res. Commun. 395:395-400.
13. Diaz-Moralli S, Ramos-Montoya A, Marin S, Fernandez-Alvarez A, Casado M, Cascante M. 2012. Target metabolomics revealed complementary roles of hexose- and pentose-phosphates in the regulation of carbohydrate-dependent gene expression. Am. J. Physiol. Endocrinol. Metab. 303:E234-E242.
14. Bricambert J, Miranda J, Benhamed F, Girard J, Postic C, Dentin R. 2010. Salt-inducible kinase 2 links transcriptional coactivator p300 phosphorylation to the prevention of ChREBP-dependent hepatic steatosis in mice. J. Clin. Invest. 120:4316-4331.
15. Guinez C, Filhoulaud G, Rayah-Benhamed F, Marmier S, Dubuquoy C, Dentin R, Moldes M, Burnol A, Yang X, Lefebvre T, Girard J, Postic C. 2011. O-GlcNAcylation increases ChREBP protein content and transcriptional activity in the liver. Diabetes 60:1399-1413.
16. Sakiyama H, Fujiwara N, Noguchi T, Eguchi H, Yoshihara D, Uyeda K, Suzuki K. 2010. The role of O-linked GlcNAc modification on the glucose response of ChREBP. Biochem. Biophys. Res. Commun. 402:784-789.
17. Adamson AW, Suchankova G, Rufo C, Nakamura MT, Teran-Garcia M, Clarke SD, Gettys TW. 2006. Hepatocyte nuclear factor-4alpha contributes to carbohydrate-induced transcriptional activation of hepatic fatty acid synthase. Biochem. J. 399:285-295.
18. Cha J, Repa JJ. 2007. The liver X receptor (LXR) and hepatic lipogenesis. The carbohydrate-response element-binding protein is a target gene of LXR. J. Biol. Chem. 282:743-751.
19. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. 2009. Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89:147-191.
20. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B. 1999. Identification of a nuclear receptor for bile acids. Science 284:1362-1365.
21. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD, Lehmann JM. 1999. Bile acids: natural ligands for an orphan nuclear receptor. Science 284:1365-1368.
22. Wang H, Chen J, Hollister K, Sowers LC, Forman BM. 1999. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol. Cell 3:543-553.
23. Lambert G, Amar MJA, Guo G, Brewer HBJ, Gonzalez FJ, Sinal CJ. 2003. The farnesoid X-receptor is an essential regulator of cholesterol homeostasis. J. Biol. Chem. 278:2563-2570.
24. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. 2000. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102:731-744.
25. Cariou B, van Harmelen K, Duran-Sandoval D, van Dijk T, Grefhorst A, Bouchaert E, Fruchart J, Gonzalez FJ, Kuipers F, Staels B. 2005. Transient impairment of the adaptive response to fasting in FXR-deficient mice. FEBS Lett. 579:4076-4080.
26. Cariou B, van Harmelen K, Duran-Sandoval D, van Dijk TH, Grefhorst A, Abdelkarim M, Caron S, Torpier G, Fruchart J, Gonzalez FJ, Kuipers F, Staels B. 2006. The farnesoid X receptor modulates adiposity and peripheral insulin sensitivity in mice. J. Biol. Chem. 281:11039-11049.
27. Ma K, Saha PK, Chan L, Moore DD. 2006. Farnesoid X receptor is essential for normal glucose homeostasis. J. Clin. Invest. 116:1102-1109.
28. Prawitt J, Abdelkarim M, Stroeve JHM, Popescu I, Duez H, Velagapudi VR, Dumont J, Bouchaert E, van Dijk TH, Lucas A, Dorchies E, Daoudi M, Lestavel S, Gonzalez FJ, Oresic M, Cariou B, Kuipers F, Caron S, Staels B. 2011. Farnesoid X receptor deficiency improves glucose homeostasis in mouse models of obesity. Diabetes 60:1861-1871.
29. Duran-Sandoval D, Mautino G, Martin G, Percevault F, Barbier O, Fruchart J, Kuipers F, Staels B. 2004. Glucose regulates the expression of the farnesoid X receptor in liver. Diabetes 53:890-898.
30. Duran-Sandoval D, Cariou B, Percevault F, Hennuyer N, Grefhorst A, van Dijk TH, Gonzalez FJ, Fruchart J, Kuipers F, Staels B. 2005. The farnesoid X receptor modulates hepatic carbohydrate metabolism during the fasting-refeeding transition. J. Biol. Chem. 280:29971-29979.
31. Samanez CH, Caron S, Briand O, Dehondt H, Duplan I, Kuipers F, Hennuyer N, Clavey V, Staels B. 2012. The human hepatocyte cell lines IHH and HepaRG: models to study glucose, lipid and lipoprotein metabolism. Arch. Physiol. Biochem. 118:102-111.
32. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
33. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, Guyomard C, Lucas J, Trepo C, Guguen-Guillouzo C. 2002. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. U. S. A. 99:15655-15660.
34. Schippers IJ, Moshage H, Roelofsen H, Müller M, Heymans HS, Ruiters M, Kuipers F. 1997. Immortalized human hepatocytes as a tool for the study of hepatocytic (de-)differentiation. Cell Biol. Toxicol. 13:375-386.
35. Caron S, Verrijken A, Mertens I, Samanez CH, Mautino G, Haas JT, Duran-Sandoval D, Prawitt J, Francque S, Vallez E, Muhr-Tailleux A, Berard I, Kuipers F, Kuivenhoven JA, Biddinger SB, Taskinen M, Van Gaal L, Staels B. 2011. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol. 31:513-519.
36. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
37. Pellicciari R, Fiorucci S, Camaioni E, Clerici C, Costantino G, Maloney PR, Morelli A, Parks DJ, Willson TM. 2002. 6alpha-ethylchenodeoxycholic acid (6-ECDCA), a potent and selective FXR agonist endowed with anticholestatic activity. J. Med. Chem. 45:3569-3572.
38. Yamada K, Noguchi T. 1999. Nutrient and hormonal regulation of pyruvate kinase gene expression. Biochem. J. 337(Pt 1):1-11.
39. Bergot MO, Diaz-Guerra MJ, Puzenat N, Raymondjean M, Kahn A. 1992. Cis-regulation of the L-type pyruvate kinase gene promoter by glucose, insulin and cyclic AMP. Nucleic Acids Res. 20:1871-1877.
40. Burke SJ, Collier JJ, Scott DK. 2009. cAMP prevents glucose-mediated modifications of histone H3 and recruitment of the RNA polymerase II holoenzyme to the L-PK gene promoter. J. Mol. Biol. 392:578-588.
41. Cha-Molstad H, Saxena G, Chen J, Shalev A. 2009. Glucose-stimulated expression of Txnip is mediated by carbohydrate response elementbinding protein, p300, and histone H4 acetylation in pancreatic beta cells. J. Biol. Chem. 284:16898-16905.
42. Watson PJ, Fairall L, Schwabe JWR. 2012. Nuclear hormone receptor co-repressors: structure and function. Mol. Cell. Endocrinol. 348:440-449.
43. Perttilä J, Huaman-Samanez C, Caron S, Tanhuanpää K, Staels B, Yki-Järvinen H, Olkkonen VM. 2012. PNPLA3 is regulated by glucose in human hepatocytes, and its I148M mutant slows down triglyceride hydrolysis. Am. J. Physiol. Endocrinol. Metab. 302:E1063-E1069.
44. Pang S, Hsieh W, Chuang C, Chao C, Weng W, Juang H. 2009. Thioredoxin-interacting protein: an oxidative stress-related gene is upregulated by glucose in human prostate carcinoma cells. J. Mol. Endocrinol. 42:205-214.
45. Parviz F, Matullo C, Garrison WD, Savatski L, Adamson JW, Ning G, Kaestner KH, Rossi JM, Zaret KS, Duncan SA. 2003. Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nat. Genet. 34:292-296.
46. Gonzalez FJ. 2008. Regulation of hepatocyte nuclear factor 4 alphamediated transcription. Drug Metab. Pharmacokinet. 23:2-7.
47. Gineste R, Sirvent A, Paumelle R, Helleboid S, Aquilina A, Darteil R, Hum DW, Fruchart J, Staels B. 2008. Phosphorylation of farnesoid X receptor by protein kinase C promotes its transcriptional activity. Mol. Endocrinol. 22:2433-2447.
48. Pascual G, Fong AL, Ogawa S, Gamliel A, Li AC, Perissi V, Rose DW, Willson TM, Rosenfeld MG, Glass CK. 2005. A SUMOylationdependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437:759-763.
49. Li M, Yang X. 2011. A retrospective on nuclear receptor regulation of inflammation: lessons from GR and PPARs. PPAR Res. 2011:742785. doi: 10.1155/2011/742785.
50. Jeong Y, Kim D, Lee YS, Kim H, Han J, Im S, Chong HK, Kwon J, Cho Y, Kim WK, Osborne TF, Horton JD, Jun H, Ahn Y, Ahn S, Cha J. 2011. Integrated expression profiling and genome-wide analysis of ChREBP targets reveals the dual role for ChREBP in glucose-regulated gene expression. PLoS One 6:e22544. doi:10.1371/journal.pone.0022544.