Fasting-induced FGF21 is repressed by LXR activation via recruitment of an HDAC3 corepressor complex in mice

Molecular Endocrinology

Volumn 26, Issue 12, 2012, Pages 1980-1990

  Archer, Amena ^a   Venteclef, Nicolas ^b,c,d   Mode, Agneta ^a   Pedrelli, Matteo ^a,e   Gabbi, Chiara ^f   Clément, Karine ^b,c,d   Parini, Paolo ^a,e   Gustafsson, Jan Åke ^a,f   Korach André, Marion ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Institute of Cardiometabolism and Nutrition   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^f University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; CHOLESTEROL; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 21; HISTONE DEACETYLASE 3; INSULIN; LIVER X RECEPTOR; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; RETINOID RELATED ORPHAN RECEPTOR ALPHA; REV PROTEIN; TRIACYLGLYCEROL;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; GENOTYPE; INSULIN SENSITIVITY; KETOGENESIS; LIPID LIVER LEVEL; MALE; METABOLIC PARAMETERS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; BENZOATES; BENZYLAMINES; FASTING; FIBROBLAST GROWTH FACTORS; GLUCOSE; HISTONE DEACETYLASES; HOMEOSTASIS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; ORPHAN NUCLEAR RECEPTORS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

ANIMALIA; MUS;

EID: 84870312300     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1151     Document Type: Article

References (53)

1. Pilkis SJ, Granner DK 1992 Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol 54: 885-909
2. 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
3. Rutter GA 2000 Diabetes: the importance of the liver. Curr Biol 10:R736-R738
4. Laffitte BA, Chao LC, Li J, Walczak R, Hummasti S, Joseph SB, Castrillo A, Wilpitz DC, Mangelsdorf DJ, Collins JL, Saez E, Tontonoz P 2003 Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc Natl Acad Sci USA 100:5419-5424
5. Cao G, Liang Y, Broderick CL, Oldham BA, Beyer TP, Schmidt RJ, Zhang Y, Stayrook KR, Suen C, Otto KA, Miller AR, Dai J, Foxworthy P, Gao H, Ryan TP, Jiang XC, Burris TP, Eacho PI, Etgen GJ 2003 Antidiabetic action of a liver X receptor agonist mediated by inhibition of hepatic gluconeogenesis. J Biol Chem 278:1131-1136
6. Geyeregger R, Zeyda M, Stulnig TM 2006 Liver X receptors in cardiovascular and metabolic disease. Cell Mol Life Sci 63:524-539
7. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, Li L, Schwendner S, Wang S, Thoolen M, Mangelsdorf DJ, Lustig KD, Shan B 2000 Role of LXRs in control of lipogenesis. Genes Dev 14:2831-2838
8. Tobin KA, Ulven SM, Schuster GU, Steineger HH, Andresen SM, Gustafsson JA, Nebb HI 2002 Liver X receptors as insulin-mediating factors in fatty acid and cholesterol biosynthesis. J Biol Chem 277:10691-10697
9. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, Sandusky GE, Hammond LJ, Moyers JS, Owens RA, Gromada J, Brozinick JT, Hawkins ED, Wroblewski VJ, Li DS, Mehrbod F, Jaskunas SR, Shanafelt AB 2005 FGF-21 as a novel metabolic regulator. J Clin Invest 115:1627-1635
10. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, Hansen BC, Shanafelt AB, Etgen GJ 2007 The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 148:774-781
11. Mashili FL, Austin RL, Deshmukh AS, Fritz T, Caidahl K, Bergdahl K, Zierath JR, Chibalin AV, Moller DE, Kharitonenkov A, Krook A 2011 Direct effects of FGF21 on glucose uptake in human skeletal muscle: implications for type 2 diabetes and obesity. Diabetes Metab Res Rev 27:286-297
12. Wente W, Efanov AM, Brenner M, Kharitonenkov A, Köster A, Sandusky GE, Sewing S, Treinies I, Zitzer H, Gromada J 2006 Fibroblast growth factor-21 improves pancreatic +-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways. Diabetes 55:2470-2478
13. Zhang X, Yeung DC, Karpisek M, Stejskal D, Zhou ZG, Liu F, Wong RL, Chow WS, Tso AW, Lam KS, Xu A 2008 Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 57:1246-1253
14. Fon Tacer K, Bookout AL, Ding X, Kurosu H, John GB, Wang L, Goetz R, Mohammadi M, Kuro-o M, Mangelsdorf DJ, Kliewer SA 2010 Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol 24:2050-2064
15. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, Li Y, Goetz R, Mohammadi M, Esser V, Elmquist JK, Gerard RD, Burgess SC, Hammer RE, Mangelsdorf DJ, Kliewer SA 2007 Endocrine regulation of the fasting response by PPAR+-mediated induction of fibroblast growth factor 21. Cell Metab 5:415-425
16. Coskun T, Bina HA, Schneider MA, Dunbar JD, Hu CC, Chen Y, Moller DE, Kharitonenkov A 2008 Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 149:6018-6027
17. Li X, Ge H, Weiszmann J, Hecht R, Li YS, Véniant MM, Xu J, Wu X, Lindberg R, Li Y 2009 Inhibition of lipolysis may contribute to the acute regulation of plasma FFA and glucose by FGF21 in ob/ob mice. FEBS Lett 583:3230-3234
18. Badman MK, Koester A, Flier JS, Kharitonenkov A, Maratos-Flier E 2009 Fibroblast growth factor 21-deficient mice demonstrate impaired adaptation to ketosis. Endocrinology 150:4931-4940
19. Muise ES, Azzolina B, Kuo DW, El-Sherbeini M, Tan Y, Yuan X, Mu J, Thompson JR, Berger JP, Wong KK 2008 Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferator-activated receptor gamma and altered metabolic states. Mol Pharmacol 74:403-412
20. Estall JL, Ruas JL, Choi CS, Laznik D, Badman M, Maratos-Flier E, Shulman GI, Spiegelman BM 2009 PGC-1+ negatively regulates hepatic FGF21 expression by modulating the heme/Rev-Erb(+) axis. Proc Natl Acad Sci USA 106:22510-22515
21. Alberti S, Schuster G, Parini P, Feltkamp D, Diczfalusy U, Rudling M, Angelin B, Björkhem I, Pettersson S, Gustafsson JA 2001 Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXR+-deficient mice. J Clin Invest 107:565-573
22. Gabbi C, Kim HJ, Hultenby K, Bouton D, Toresson G, Warner M, Gustafsson JA 2008 Pancreatic exocrine insufficiency in LXR++/+ mice is associated with a reduction in aquaporin-1 expression. Proc Natl Acad Sci USA 105:15052-15057
23. Yin L, Wu N, Curtin JC, Qatanani M, Szwergold NR, Reid RA, Waitt GM, Parks DJ, Pearce KH, Wisely GB, Lazar MA 2007 Rev-erb+, a heme sensor that coordinates metabolic and circadian pathways. Science 318:1786-1789
24. Wada T, Kang HS, Angers M, Gong H, Bhatia S, Khadem S, Ren S, Ellis E, Strom SC, Jetten AM, Xie W 2008 Identification of oxysterol 7+-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor + (ROR+) (NR1F1) target gene and a functional cross-talk between ROR+ and liver X receptor (NR1H3). Mol Pharmacoly 73:891-899
25. Uebanso T, Taketani Y, Yamamoto H, Amo K, Tanaka S, Arai H, Takei Y, Masuda M, Yamanaka-Okumura H, Takeda E 2012 Liver X receptor negatively regulates fibroblast growth factor 21 in the fatty liver induced by cholesterol-enriched diet. J Nutr Biochem 23:785-790
26. Korach-André M, Archer A, Gabbi C, Barros RP, Pedrelli M, Steffensen KR, Pettersson AT, Laurencikiene J, Parini P, Gustafsson JÅ 2011, Liver-X receptors regulate de novo lipogenesis in a tissue specific manner in C57Bl/6 female mice. Am J Physiol Endocrinol Metab 301:E210-E222
27. Folch J, Lees M, Sloane Stanley GH 1957 A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
28. Jakobsson T, Venteclef N, Toresson G, Damdimopoulos AE, Ehrlund A, Lou X, Sanyal S, Steffensen KR, Gustafsson JA, Treuter E 2009 GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol Cell 34:510-518
29. Pehkonen P, Welter-Stahl L, Diwo J, Ryynänen J, Wienecke-Baldacchino A, Heikkinen S, Treuter E, Steffensen KR, Carlberg C 2012 Genome-wide landscape of liver X receptor chromatin binding and gene regulation in human macrophages. BMC Genomics 13:50
30. Hotta Y, Nakamura H, Konishi M, Murata Y, Takagi H, Matsumura S, Inoue K, Fushiki T, ItohN2009 Fibroblast growth factor
31. Marinescu VD, Kohane IS, Riva A 2005 The MAPPER database: a multi-genome catalog of putative transcription factor binding sites. Nucleic Acids Res 33:D91-D97
32. Sandelin A, Wasserman WW 2005 Prediction of nuclear hormone receptor response elements. Mol Endocrinol 19:595-606
33. Wang Y, Solt LA, Burris TP 2010 Regulation of FGF21 expression and secretion by retinoic acid receptor-related orphan receptor alpha. J Biol Chem 285:15668-15673
34. Raghuram S, Stayrook KR, Huang P, Rogers PM, Nosie AK, Mc-Clure DB, Burris LL, Khorasanizadeh S, Burris TP, Rastinejad F 2007 Identification of heme as the ligand for the orphan nuclear receptors REV-ERB+ and REV-ERB+. Nat Struct Mol Biol 14: 1207-1213
35. Houck KA, Borchert KM, Hepler CD, Thomas JS, Bramlett KS, Michael LF, Burris TP 2004 T0901317 is a dual LXR/FXR agonist. Mol Genet Metab 83:184-187
36. Mitro N, Vargas L, Romeo R, Koder A, Saez E 2007 T0901317 is a potent PXR ligand: implications for the biology ascribed to LXR. FEBS Lett 581:1721-1726
37. Kumar N, Solt LA, Conkright JJ, Wang Y, Istrate MA, Busby SA, Garcia-Ordonez RD, Burris TP, Griffin PR 2010 The benzenesulfoamide T0901317 [N-(2,2,2-trifluoroethyl)-N-[4-[2,2,2-trifluoro-1-hydroxy-1-(trifluoromethyl)ethy l]phenyl]-benzenesulfonamide] is a novel retinoic acid receptor-related orphan receptor-+/+ inverse agonist. Mol Pharmacol 77:228-236
38. Boergesen M, Pedersen TÅ, Gross B, van Heeringen SJ, Hagenbeek D, Bindesboll C, Caron S, Lalloyer F, Steffensen KR, Nebb HI, Gustafsson JÅ, Stunnenberg HG, Staels B, Mandrup S 2012 Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor + in mouse liver reveals extensive sharing of binding sites. Mol Cell Biol 32:852-867
39. Blaschke F, Takata Y, Caglayan E, Collins A, Tontonoz P, Hsueh WA, Tangirala RK 2006 A nuclear receptor corepressor-dependent pathway mediates suppression of cytokine-induced C-reactive protein gene expression by liver X receptor. Circ Res 99:e88-e99
40. Ghisletti S, Huang W, Ogawa S, Pascual G, Lin ME, Willson TM, Rosenfeld MG, Glass CK 2007 Parallel SUMOylation-dependent pathways mediate gene-and signal-specific transrepression by LXRs and PPAR+. Mol Cell 25:57-70
41. Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, Ellis E, Nilsson LM, Parini P, Jänne OA, Gustafsson JA, Steffensen KR, Treuter E 2010 GPS2-dependent corepressor/ SUMO pathways govern anti-inflammatory actions of LRH-1 and LXR+ in the hepatic acute phase response. Genes Dev 24:381-395
42. Harding HP, Atkins GB, Jaffe AB, Seo WJ, Lazar MA 1997 Transcriptional activation and repression by ROR+, an orphan nuclear receptor required for cerebellar development. Mol Endocrinol 11: 1737-1746
43. Moraitis AN, Giguère V 2003 The co-repressor hairless protects ROR+ orphan nuclear receptor from proteasome-mediated degradation. J Biol Chem 278:52511-52518
44. Guenther MG, Barak O, Lazar MA 2001 The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 21:6091-6101
45. Yu H, Wu J, Yang M, Guo J, Zheng L, Peng M, Zhang Q, Xiang Y, Cao J, Shen W 2012 Involvement of liver X receptor + in histone modifications across the target fatty acid synthase gene. Lipids 47: 249-257
46. Kininis M, Isaacs GD, Core LJ, Hah N, KrausWL2009 Postrecruitment regulation of RNA polymerase II directs rapid signaling responses at the promoters of estrogen target genes. Mol Cell Biol 29:1123-1133
47. Anthonisen EH, Berven L, Holm S, Nygård M, Nebb HI, Gronning-Wang LM 2010 Nuclear receptor liver X receptor is O-GlcNAcmodified in response to glucose. J Biol Chem 285:1607-1615
48. Cha JY, 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
49. Denechaud PD, Bossard P, Lobaccaro JM, Millatt L, Staels B, Girard J, Postic C 2008 ChREBP, but not LXRs, is required for the induction of glucose-regulated genes in mouse liver. J Clin Invest 118:956-964
50. Korach-André M, Parini P, Larsson L, Arner A, Steffensen KR, Gustafsson JA 2010 Separate and overlapping metabolic functions of LXR+ and LXR+ in C57Bl/6 female mice. Am J Physiol Endocrinol Metab 298:E167-E178
51. Oosterveer MH, van Dijk TH, Grefhorst A, Bloks VW, Havinga R, Kuipers F, Reijngoud DJ 2008 Lxr+ deficiency hampers the hepatic adaptive response to fasting in mice. J Biol Chem 283:25437-25445
52. Laffel L 1999 Ketone bodies: a review of physiology, pathophysiology and application of monitoring to diabetes. Diabetes Metab Res Rev 15:412-426
53. Gerin I, Dolinsky VW, Shackman JG, Kennedy RT, Chiang SH, Burant CF, Steffensen KR, Gustafsson JA, MacDougald OA 2005 LXR+ is required for adipocyte growth, glucose homeostasis, and + cell function. J Biol Chem 280:23024-23031