Retinoid acid-related orphan receptor γ, RORγ, participates in diurnal transcriptional regulation of lipid metabolic genes

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10448-10459

  Takeda, Yukimasa ^a   Kang, Hong Soon ^a   Lih, Fred B ^a   Jiang, Hongfeng ^b   Blaner, William S ^b   Jetten, Anton M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN RECEPTOR 2; BILE ACID; CELL PROTEIN; CHOLESTEROL; FATTY ACID; FATTY ACID TRANSPORTER; HIGH DENSITY LIPOPROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN; RETINOIC ACID RELATED ORPHAN RECEPTOR RESPONSE ELEMENT; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ACYLTRANSFERASE; FATTY ACID ELONGASES; INSIG2 PROTEIN, MOUSE; MEMBRANE PROTEIN;

ADIPOR2 GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD36 GENE; CONTROLLED STUDY; CYP27A1 GENE; CYP7B1 GENE; CYP8B1 GENE; DOWN REGULATION; ELOVL3 GENE; ELOVL5 GENE; ELOVL6 GENE; FASN GENE; GENE; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HISTONE ACETYLATION; HMG COA REDUCTASE GENE; HSD3B5 GENE; INSIG2A GENE; LIPC GENE; LIPID COMPOSITION; LIPID HOMEOSTASIS; LIPID METABOLISM; MALE; MOUSE; NOCTURNIN GENE; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; C57BL MOUSE; CIRCADIAN RHYTHM; DNA RESPONSIVE ELEMENT; GENETIC TRANSCRIPTION; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; PHYSIOLOGY;

MUS;

ACETYLTRANSFERASES; ANIMALS; BILE ACIDS AND SALTS; CIRCADIAN CLOCKS; GENE EXPRESSION REGULATION; LIPID METABOLISM; LIVER; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; RESPONSE ELEMENTS; TRANSCRIPTION, GENETIC; TRIGLYCERIDES;

EID: 84921371592     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku766     Document Type: Article

References (45)

1. Jetten,A.M. (2009) Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl. Recept. Signal., 7, e003.
2. Solt,L.A. and Burris,T.P. (2012) Action of RORs and their ligands in (patho)physiology. Trends Endocrinol.Metab., 23, 619-627.
3. Huh,J.R. and Littman,D.R. (2012) Small molecule inhibitors of RORgammat: targeting Th17 cells and other applications. Eur. J. Immunol., 42, 2232-2237.
4. Bookout,A.L., Jeong,Y., Downes,M., Yu,R.T., Evans,R.M. and Mangelsdorf,D.J. (2006) Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell, 126, 789-799.
5. Medvedev,A., Yan,Z.H., Hirose,T., Giguere,V. and Jetten,A.M. (1996) Cloning of a cDNA encoding the murine orphan receptor RZR/ROR gamma and characterization of its response element. Gene, 181, 199-206.
6. Bass,J. and Takahashi,J.S. (2010) Circadian integration of metabolism and energetics. Science, 330, 1349-1354.
7. Duez,H. and Staels,B. (2010) Nuclear receptors linking circadian rhythms and cardiometabolic control. Arterioscler. Thromb. Vasc. Biol., 30, 1529-1534.
8. Eckel-Mahan,K. and Sassone-Corsi,P. (2013) Metabolism and the circadian clock converge. Physiol. Rev., 93, 107-135.
9. Asher,G. and Schibler,U. (2011) Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab., 13, 125-137.
10. Rey,G. and Reddy,A.B. (2013) Connecting cellular metabolism to circadian clocks. Trends Cell Biol., 23, 234-241.
11. Maury,E., Hong,H.K. and Bass,J. (2014) Circadian disruption in the pathogenesis of metabolic syndrome. In: Diabetes Metab, doi:10.1016/j.diabet.2013.12.005.
12. Hatori,M., Vollmers,C., Zarrinpar,A., DiTacchio,L., Bushong,E.A., Gill,S., Leblanc,M., Chaix,A., Joens,M., Fitzpatrick,J.A. et al. (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab., 15, 848-860.
13. Yang,X., Downes,M., Yu,R.T., Bookout,A.L., He,W., Straume,M., Mangelsdorf,D.J. and Evans,R.M. (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell, 126, 801-810.
14. Liu,A.C., Tran,H.G., Zhang,E.E., Priest,A.A., Welsh,D.K. and Kay,S.A. (2008) Redundant function of REV-ERBalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet., 4, e1000023.
15. Ueda,H.R., Hayashi,S., Chen,W., Sano,M., Machida,M., Shigeyoshi,Y., Iino,M. and Hashimoto,S. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet., 37, 187-192.
16. Takeda,Y., Jothi,R., Birault,V. and Jetten,A.M. (2012) RORgamma directly regulates the circadian expression of clock genes and downstream targets in vivo. Nucleic Acids Res., 40, 8519-8535.
17. Cho,H., Zhao,X., Hatori,M., Yu,R.T., Barish,G.D., Lam,M.T., Chong,L.W., DiTacchio,L., Atkins,A.R., Glass,C.K. et al. (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature, 485, 123-127.
18. Mongrain,V., Ruan,X., Dardente,H., Fortier,E.E. and Cermakian,N. (2008) Clock-dependent and independent transcriptional control of the two isoforms from the mouse Rorgamma gene. Genes Cells, 13, 1197-1210.
19. Guillaumond,F., Dardente,H., Giguere,V. and Cermakian,N. (2005) Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms, 20, 391-403.
20. Jetten,A.M., Kang,H.S. and Takeda,Y. (2013) Retinoic acid-related orphan receptors alpha and gamma: key regulators of lipid/glucose metabolism, inflammation, and insulin sensitivity. Front. Endocrinol., 4, 1-8.
21. Takeda,Y., Kang,H.S., Angers,M. and Jetten,A.M. (2011) Retinoic acid-related orphan receptor gamma directly regulates neuronal PAS domain protein 2 transcription in vivo. Nucleic Acids Res., 39, 4769-4782.
22. Takeda,Y., Kang,H.S., Freudenberg,J., DeGraff,L.M., Jothi,R. and Jetten,A.M. (2014) Retinoic acid-rrelated orphan receptor gamma (RORgamma): a novel participant in the diurnal regulation of hepatic gluconeogenesis and insulin sensitivity. PLoS Genet., 10, e1004331.
23. Kurebayashi,S., Ueda,E., Sakaue,M., Patel,D.D., Medvedev,A., Zhang,F. and Jetten,A.M. (2000) Retinoid-related orphan receptor gamma (RORgamma) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl. Acad. Sci. U.S.A., 97, 10132-10137.
24. Pathak,P., Li,T. and Chiang,J.Y. (2013) Retinoic acid-related orphan receptor alpha regulates diurnal rhythm and fasting induction of sterol 12alpha-hydroxylase in bile acid synthesis. J. Biol. Chem., 288, 37154-37165.
25. Takeda,Y. and Jetten,A.M. (2013) Prospero-related homeobox 1 (Prox1) functions as a novel modulator of retinoic acid-related orphan receptors alpha-and gamma-mediated transactivation. Nucleic Acids Res., 41, 6992-7008.
26. Wada,T., Kang,H.S., Angers,M., Gong,H., Bhatia,S., Khadem,S., Ren,S., Ellis,E., Strom,S.C., Jetten,A.M. et al. (2008) Identification of oxysterol 7alpha-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor alpha (RORalpha) (NR1F1) target gene and a functional cross-talk between RORalpha and liver X receptor (NR1H3). Mol. Pharmacol., 73, 891-899.
27. Dong,X.Y. and Tang,S.Q. (2010) Insulin-induced gene: a new regulator in lipid metabolism. Peptides, 31, 2145-2150.
28. Shao,W. and Espenshade,P.J. (2012) Expanding roles for SREBP in metabolism. Cell Metab., 16, 414-419.
29. Le Martelot,G., Claudel,T., Gatfield,D., Schaad,O., Kornmann,B., Sasso,G.L., Moschetta,A. and Schibler,U. (2009) REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol., 7, e1000181.
30. Engelking,L.J., Liang,G., Hammer,R.E., Takaishi,K., Kuriyama,H., Evers,B.M., Li,W.P., Horton,J.D., Goldstein,J.L. and Brown,M.S. (2005) Schoenheimer effect explained-feedback regulation of cholesterol synthesis in mice mediated by Insig proteins. J. Clin. Invest., 115, 2489-2498.
31. Clugston,R.D., Jiang,H., Lee,M.X., Piantedosi,R., Yuen,J.J., Ramakrishnan,R., Lewis,M.J., Gottesman,M.E., Huang,L.S., Goldberg,I.J. et al. (2011) Altered hepatic lipid metabolism in C57BL/6 mice fed alcohol: a targeted lipidomic and gene expression study. J. Lipid Res., 52, 2021-2031.
32. Calkin,A.C. and Tontonoz,P. (2012) Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nature Rev. Mol. Cell Biol., 13, 213-224.
33. Handschin,C. and Meyer,U.A. (2005) Regulatory network of lipid-sensing nuclear receptors: roles for CAR, PXR, LXR, and FXR. Arch. Biochem. Biophys., 433, 387-396.
34. Kidani,Y. and Bensinger,S.J. (2012) Liver X receptor and peroxisome proliferator-activated receptor as integrators of lipid homeostasis and immunity. Immunol. Rev., 249, 72-83.
35. Bass,J. (2012) Circadian topology of metabolism. Nature, 491, 348-356.
36. Kitazawa,M. (2013) Circadian rhythms, metabolism, and insulin sensitivity: transcriptional networks in animal models. Curr. Diab. Rep., 13, 223-228.
37. Koike,N., Yoo,S.H., Huang,H.C., Kumar,V., Lee,C., Kim,T.K. and Takahashi,J.S. (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science, 338, 349-354.
38. Jin,L., Martynowski,D., Zheng,S., Wada,T., Xie,W. and Li,Y. (2010) Structural basis for hydroxycholesterols as natural ligands of orphan nuclear receptor RORgamma. Mol. Endocrinol., 24, 923-929.
39. Yellaturu,C.R., Deng,X., Park,E.A., Raghow,R. and Elam,M.B. (2009) Insulin enhances the biogenesis of nuclear sterol regulatory element-binding protein (SREBP)-1c by posttranscriptional down-regulation of Insig-2A and its dissociation from SREBP cleavage-activating protein (SCAP).SREBP-1c complex. J. Biol. Chem., 284, 31726-31734.
40. Peterson,T.R., Sengupta,S.S., Harris,T.E., Carmack,A.E., Kang,S.A., Balderas,E., Guertin,D.A.,Madden,K.L., Carpenter,A.E., Finck,B.N. et al. (2011) mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell, 146, 408-420.
41. Radominska,A., Comer,K.A., Zimniak,P., Falany,J., Iscan,M. and Falany,C.N. (1990) Human liver steroid sulphotransferase sulphates bile acids. Biochem. J., 272, 597-604.
42. Kang,H.S., Angers,M., Beak,J.Y., Wu,X., Gimble,J.M., Wada,T., Xie,W., Collins,J.B., Grissom,S.F. and Jetten,A.M. (2007) Gene expression profiling reveals a regulatory role for ROR alpha and ROR gamma in phase I and phase II metabolism. Physiol. Genomics, 31, 281-294.
43. Ou,Z., Shi,X., Gilroy,R.K., Kirisci,L., Romkes,M., Lynch,C., Wang,H., Xu,M., Jiang,M., Ren,S. et al. (2013) Regulation of the human hydroxysteroid sulfotransferase (SULT2A1) by RORalpha and RORgamma and its potential relevance to human liver diseases. Mol. Endocrinol., 27, 106-115.
44. Meissburger,B., Ukropec,J., Roeder,E., Beaton,N., Geiger,M., Teupser,D., Civan,B., Langhans,W., Nawroth,P.P., Gasperikova,D. et al. (2011) Adipogenesis and insulin sensitivity in obesity are regulated by retinoid-related orphan receptor gamma. EMBO Mol. Med., 3, 637-651.
45. Tinahones,F.J., Moreno-Santos,I., Vendrell,J., Chacon,M.R., Garrido-Sanchez,L., Garcia-Fuentes,E. and Macias-Gonzalez,M. (2012) The retinoic acid receptor-related orphan nuclear receptor gamma1 (RORgamma1): a novel player determinant of insulin sensitivity in morbid obesity. Obesity, 20, 488-497.