Retinoid-related orphan receptor alpha and the regulation of lipid homeostasis

Journal of Steroid Biochemistry and Molecular Biology

Volumn 130, Issue 3-5, 2012, Pages 159-168

  Fitzsimmons, Rebecca L ^a   Lau, Patrick ^a   Muscat, George E O ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Lipogenesis; Lipoprotein metabolism; Metabolism; Nuclear hormone receptor; ROR ; Staggerer

Indexed keywords

N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR BETA; RETINOID RELATED ORPHAN RECEPTOR GAMMA;

ADIPOSE TISSUE; CIRCADIAN RHYTHM; DNA BINDING; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; HOMEOSTASIS; HUMAN; INFLAMMATION; LIGAND BINDING; LIPID HOMEOSTASIS; LIPID METABOLISM; LIVER; METABOLIC DISORDER; MOLECULAR INTERACTION; NONHUMAN; OBESITY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SKELETAL MUSCLE; TISSUE DISTRIBUTION;

ADIPOSE TISSUE; ANIMALS; FEMALE; HOMEOSTASIS; HUMANS; INFLAMMATION; LIPID METABOLISM; LIPID METABOLISM DISORDERS; LIVER; MALE; MICE; MUSCLE, SKELETAL; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1;

EID: 84861189139     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.06.009     Document Type: Review

References (104)

1. A.R. Chopra, J.F. Louet, P. Saha, J. An, F. Demayo, J. Xu, B. York, S. Karpen, M. Finegold, D. Moore, L. Chan, C.B. Newgard, and B.W. O'Malley Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke's disease Science 322 5906 2008 1395 1399 (Pubitemid 352775254)
2. P. Lau, R.L. Fitzsimmons, M.A. Pearen, M.J. Watt, and G.E. Muscat Homozygous staggerer (sg/sg) mice display improved insulin sensitivity and enhanced glucose uptake in skeletal muscle Diabetologia 54 5 2011 1169 1180
3. H.S. Kang, M. Angers, J.Y. Beak, X. Wu, J.M. Gimble, T. Wada, W. Xie, J.B. Collins, S.F. Grissom, and A.M. Jetten Gene expression profiling reveals a regulatory role for ROR alpha and ROR gamma in phase I and phase II metabolism Physiol. Genomics 31 2 2007 281 294 (Pubitemid 350014406)
4. T. Wada, H.S. Kang, M. Angers, H. Gong, S. Bhatia, S. Khadem, S. Ren, E. Ellis, S.C. Strom, A.M. Jetten, and W. Xie 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 3 2008 891 899 (Pubitemid 351397893)
5. M. Becker-Andre, E. Andre, and J.F. DeLamarter Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences Biochem. Biophys. Res. Commun. 194 3 1993 1371 1379 (Pubitemid 23255034)
6. V. Giguere, M. Tini, G. Flock, E. Ong, R.M. Evans, and G. Otulakowski Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors Genes Dev. 8 5 1994 538 553
7. U. Matysiak-Scholze, and M. Nehls The structural integrity of ROR alpha isoforms is mutated in staggerer mice: cerebellar coexpression of ROR alpha1 and ROR alpha4 Genomics 43 1 1997 78 84 (Pubitemid 27310525)
8. V. Giguere, L.D. McBroom, and G. Flock Determinants of target gene specificity for ROR alpha 1: monomeric DNA binding by an orphan nuclear receptor Mol. Cell. Biol. 15 5 1995 2517 2526
9. C. Carlberg, R. Hooft van Huijsduijnen, J.K. Staple, J.F. DeLamarter, and M. Becker-Andre RZRs, a new family of retinoid-related orphan receptors that function as both monomers and homodimers Mol. Endocrinol. 8 6 1994 757 770 (Pubitemid 24179668)
10. E. Andre, K. Gawlas, and M. Becker-Andre A novel isoform of the orphan nuclear receptor RORbeta is specifically expressed in pineal gland and retina Gene 216 2 1998 277 283 (Pubitemid 28408189)
11. T. Hirose, R.J. Smith, and A.M. Jetten ROR gamma: the third member of ROR/RZR orphan receptor subfamily that is highly expressed in skeletal muscle Biochem. Biophys. Res. Commun. 205 3 1994 1976 1983
12. S. Nakagawa, M. Watanabe, and Y. Inoue Prominent expression of nuclear hormone receptor ROR alpha in Purkinje cells from early development Neurosci. Res. 28 2 1997 177 184 (Pubitemid 27267827)
13. S. Sashihara, P.A. Felts, S.G. Waxman, and T. Matsui Orphan nuclear receptor ROR alpha gene: isoform-specific spatiotemporal expression during postnatal development of brain Brain Res. Mol. Brain Res. 42 1 1996 109 117 (Pubitemid 26345412)
14. M. Steinmayr, E. Andre, F. Conquet, L. Rondi-Reig, N. Delhaye-Bouchaud, N. Auclair, H. Daniel, F. Crepel, J. Mariani, C. Sotelo, and M. Becker-Andre staggerer phenotype in retinoid-related orphan receptor alpha-deficient mice Proc. Natl. Acad. Sci. U.S.A. 95 7 1998 3960 3965 (Pubitemid 28173236)
15. N. Schaeren-Wiemers, E. Andre, J.P. Kapfhammer, and M. Becker-Andre The expression pattern of the orphan nuclear receptor RORbeta in the developing and adult rat nervous system suggests a role in the processing of sensory information and in circadian rhythm Eur. J. Neurosci. 9 12 1997 2687 2701 (Pubitemid 28082958)
16. E. Andre, F. Conquet, M. Steinmayr, S.C. Stratton, V. Porciatti, and M. Becker-Andre Disruption of retinoid-related orphan receptor beta changes circadian behavior, causes retinal degeneration and leads to vacillans phenotype in mice EMBO J. 17 14 1998 3867 3877 (Pubitemid 28333973)
17. R. Baler, S. Coon, and D.C. Klein Orphan nuclear receptor RZRbeta: cyclic AMP regulates expression in the pineal gland Biochem. Biophys. Res. Commun. 220 3 1996 975 978 (Pubitemid 26198624)
18. C. Carlberg, and I. Wiesenberg The orphan receptor family RZR/ROR, melatonin and 5-lipoxygenase: an unexpected relationship J. Pineal Res. 18 4 1995 171 178
19. L. Chow, E.M. Levine, and T.A. Reh The nuclear receptor transcription factor, retinoid-related orphan receptor beta, regulates retinal progenitor proliferation Mech. Dev. 77 2 1998 149 164 (Pubitemid 28545167)
20. M.A. Ortiz, F.J. Piedrafita, M. Pfahl, and R. Maki TOR: a new orphan receptor expressed in the thymus that can modulate retinoid and thyroid hormone signals Mol. Endocrinol. 9 12 1995 1679 1691
21. Y.W. He, M.L. Deftos, E.W. Ojala, and M.J. Bevan RORgamma t, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in T cells Immunity 9 6 1998 797 806 (Pubitemid 29024459)
22. G. Eberl, S. Marmon, M.J. Sunshine, P.D. Rennert, Y. Choi, and D.R. Littman An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells Nat. Immunol. 5 1 2004 64 73 (Pubitemid 38081470)
23. I.I. Ivanov, G.E. Diehl, and D.R. Littman Lymphoid tissue inducer cells in intestinal immunity Curr. Top. Microbiol. Immunol. 308 2006 59 82 (Pubitemid 47400297)
24. A.M. Jetten, S. Kurebayashi, and E. Ueda The ROR nuclear orphan receptor subfamily: critical regulators of multiple biological processes Prog. Nucleic Acid Res. Mol. Biol. 69 2001 205 247 (Pubitemid 33804679)
25. A.N. Moraitis, and V. Giguere Transition from monomeric to homodimeric DNA binding by nuclear receptors: identification of RevErbAalpha determinants required for RORalpha homodimer complex formation Mol. Endocrinol. 13 3 1999 431 439 (Pubitemid 29113875)
26. L.D. McBroom, G. Flock, and V. Giguere The nonconserved hinge region and distinct amino-terminal domains of the ROR alpha orphan nuclear receptor isoforms are required for proper DNA bending and ROR alpha-DNA interactions Mol. Cell. Biol. 15 2 1995 796 808
27. E. Raspe, G. Mautino, C. Duval, C. Fontaine, H. Duez, O. Barbier, D. Monte, J. Fruchart, J.C. Fruchart, and B. Staels Transcriptional regulation of human Rev-erbalpha gene expression by the orphan nuclear receptor retinoic acid-related orphan receptor alpha J. Biol. Chem. 277 51 2002 49275 49281 (Pubitemid 36014356)
28. M.H. Hsu, C.N. Palmer, W. Song, K.J. Griffin, and E.F. Johnson A carboxyl-terminal extension of the zinc finger domain contributes to the specificity and polarity of peroxisome proliferator-activated receptor DNA binding J. Biol. Chem. 273 43 1998 27988 27997 (Pubitemid 28496090)
29. G.B. Atkins, X. Hu, M.G. Guenther, C. Rachez, L.P. Freedman, and M.A. Lazar Coactivators for the orphan nuclear receptor RORalpha Mol. Endocrinol. 13 9 1999 1550 1557 (Pubitemid 30650595)
30. H.P. Harding, G.B. Atkins, A.B. Jaffe, W.J. Seo, and M.A. Lazar Transcriptional activation and repression by RORalpha, an orphan nuclear receptor required for cerebellar development Mol. Endocrinol. 11 11 1997 1737 1746 (Pubitemid 27435421)
31. A.M Jetten, and J.H. Joo Retinoid-related orphan receptors (RORs): roles in cellular differentiation and development Adv. Dev. Biol. 16 2006 313 355 (Pubitemid 44725707)
32. E.J. Hwang, J.M. Lee, J. Jeong, J.H. Park, Y. Yang, J.S. Lim, J.H. Kim, S.H. Baek, and K.I. Kim SUMOylation of RORalpha potentiates transcriptional activation function Biochem. Biophys.Res. Commun. 378 3 2009 513 517
33. I. Wiesenberg, M. Missbach, and C. Carlberg The potential role of the transcription factor RZR/ROR as a mediator of nuclear melatonin signaling Restor. Neurol. Neurosci. 12 2-3 1998 143 150 (Pubitemid 28368295)
34. J.A. Kallen, J.M. Schlaeppi, F. Bitsch, S. Geisse, M. Geiser, I. Delhon, and B. Fournier X-ray structure of the hRORalpha LBD at 1.63 A: structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORalpha Structure 10 12 2002 1697 1707 (Pubitemid 35452576)
35. F. Bitsch, R. Aichholz, J. Kallen, S. Geisse, B. Fournier, and J.M. Schlaeppi Identification of natural ligands of retinoic acid receptor-related orphan receptor alpha ligand-binding domain expressed in Sf9 cells - a mass spectrometry approach Anal. Biochem. 323 1 2003 139 149 (Pubitemid 37393367)
36. J. Kallen, J.M. Schlaeppi, F. Bitsch, I. Delhon, and B. Fournier Crystal structure of the human RORalpha Ligand binding domain in complex with cholesterol sulfate at 2.2 J. Biol. Chem. 279 14 2004 14033 14038 (Pubitemid 38468938)
37. N. Kumar, L.A. Solt, J.J. Conkright, Y. Wang, M.A. Istrate, S.A. Busby, R.D. Garcia-Ordonez, T.P. Burris, and P.R. Griffin The benzenesulfoamide T0901317 [N-(2,2,2-trifluoroethyl)-N-[4-[2,2,2-trifluoro-1-hydroxy-1- (trifluorometh yl)ethyl]phenyl]-benzenesulfonamide] is a novel retinoic acid receptor-related orphan receptor-alpha/gamma inverse agonist Mol. Pharmacol. 77 2 2010 228 236
38. Y. Wang, N. Kumar, C. Crumbley, P.R. Griffin, and T.P. Burris A second class of nuclear receptors for oxysterols: regulation of RORalpha and RORgamma activity by 24S-hydroxycholesterol (cerebrosterol) Biochim. Biophys. Acta 1801 8 2010 917 923
39. Y. Wang, N. Kumar, L.A. Solt, T.I. Richardson, L.M. Helvering, C. Crumbley, R.D. Garcia-Ordonez, K.R. Stayrook, X. Zhang, S. Novick, M.J. Chalmers, P.R. Griffin, and T.P. Burris Modulation of retinoic acid receptor-related orphan receptor alpha and gamma activity by 7-oxygenated sterol ligands J. Biol. Chem. 285 7 2010 5013 5025
40. Y. Wang, N. Kumar, P. Nuhant, M.D. Cameron, M.A. Istrate, W.R. Roush, P.R. Griffin, and T.P. Burris Identification of SR 1078, a synthetic agonist for the orphan nuclear receptors RORalpha and RORgamma ACS Chem. Biol. 2010
41. N. Kumar, D.J. Kojetin, L.A. Solt, K.G. Kumar, P. Nuhant, D.R. Duckett, M.D. Cameron, A.A. Butler, W.R. Roush, P.R. Griffin, and T.P. Burris Identification of SR 3335 (ML-176): a synthetic RORalpha selective inverse agonist ACS Chem. Biol. 6 3 2011 218 222
42. L.A. Solt, N. Kumar, P. Nuhant, Y. Wang, J.L. Lauer, J. Liu, M.A. Istrate, T.M. Kamenecka, W.R. Roush, D. Vidovic, S.C. Schurer, J. Xu, G. Wagoner, P.D. Drew, P.R. Griffin, and T.P. Burris Suppression of TH17 differentiation and autoimmunity by a synthetic ROR ligand Nature 472 7344 2011 491 494
43. U. Diczfalusy, K.E. Olofsson, A.M. Carlsson, M. Gong, D.T. Golenbock, O. Rooyackers, U. Flaring, and H. Bjorkbacka Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide J. Lipid Res. 50 11 2009 2258 2264
44. J.G. McDonald, and D.W. Russell Editorial: 25-hydroxycholesterol: a new life in immunology J. Leukoc. Biol. 88 6 2010 1071 1072
45. B.A. Janowski, M.J. Grogan, S.A. Jones, G.B. Wisely, S.A. Kliewer, E.J. Corey, and D.J. Mangelsdorf Structural requirements of ligands for the oxysterol liver X receptors LXRalpha and LXRbeta Proc. Natl. Acad. Sci. U.S.A. 96 1 1999 266 271 (Pubitemid 29036088)
46. W. Chen, G. Chen, D.L. Head, D.J. Mangelsdorf, and D.W. Russell Enzymatic reduction of oxysterols impairs LXR signaling in cultured cells and the livers of mice Cell. Metab. 5 1 2007 73 79 (Pubitemid 44933109)
47. I. Bjorkhem Do oxysterols control cholesterol homeostasis? J. Clin. Invest. 110 6 2002 725 730
48. S.D. Jordan, M. Kruger, D.M. Willmes, N. Redemann, F.T. Wunderlich, H.S. Bronneke, C. Merkwirth, H. Kashkar, V.M. Olkkonen, T. Bottger, T. Braun, J. Seibler, and J.C. Bruning Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism Nat. Cell. Biol. 13 4 2011 434 446
49. R.E. Infante, L. Abi-Mosleh, A. Radhakrishnan, J.D. Dale, M.S. Brown, and J.L. Goldstein Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein J. Biol. Chem. 283 2 2008 1052 1063
50. C. Stehlin-Gaon, D. Willmann, D. Zeyer, S. Sanglier, A. Van Dorsselaer, J.P. Renaud, D. Moras, and R. Schule All-trans retinoic acid is a ligand for the orphan nuclear receptor ROR beta Nat. Struct. Biol. 10 10 2003 820 825 (Pubitemid 37187653)
51. P. Lau, S.J. Nixon, R.G. Parton, and G.E. Muscat RORalpha regulates the expression of genes involved in lipid homeostasis in skeletal muscle cells: caveolin-3 and CPT-1 are direct targets of ROR J. Biol. Chem. 279 35 2004 36828 36840 (Pubitemid 39129032)
52. S. Raichur, R.L. Fitzsimmons, S.A. Myers, M.A. Pearen, P. Lau, N. Eriksson, S.M. Wang, and G.E. Muscat Identification and validation of the pathways and functions regulated by the orphan nuclear receptor, ROR alpha1, in skeletal muscle Nucleic Acids Res. 38 13 2010 4296 4312
53. I. Dussault, D. Fawcett, A. Matthyssen, J.A. Bader, and V. Giguere Orphan nuclear receptor ROR alpha-deficient mice display the cerebellar defects of staggerer Mech. Dev. 70 1-2 1998 147 153 (Pubitemid 28116489)
54. D.A. Gold, P.M. Gent, and B.A. Hamilton ROR alpha in genetic control of cerebellum development: 50 staggering years Brain Res. 1140 2007 19 25 (Pubitemid 46356289)
55. B.L. Wagner, A.F. Valledor, G. Shao, C.L. Daige, E.D. Bischoff, M. Petrowski, K. Jepsen, S.H. Baek, R.A. Heyman, M.G. Rosenfeld, I.G. Schulman, and C.K. Glass Promoter-specific roles for liver X receptor/corepressor complexes in the regulation of ABCA1 and SREBP1 gene expression Mol. Cell. Biol. 23 16 2003 5780 5789 (Pubitemid 36951340)
56. D.E. Kelley Skeletal muscle triglycerides: an aspect of regional adiposity and insulin resistance Ann. N. Y. Acad. Sci. 967 2002 135 145 (Pubitemid 34721901)
57. V.T. Samuel, K.F. Petersen, and G.I. Shulman Lipid-induced insulin resistance: unravelling the mechanism Lancet 375 9733 2010 2267 2277
58. A.M. Sharma, and V.T. Chetty Obesity, hypertension and insulin resistance Acta Diabetol. 42 Suppl 1 2005 S3 S8
59. S. Raichur, P. Lau, B. Staels, and G.E. Muscat Retinoid-related orphan receptor gamma regulates several genes that control metabolism in skeletal muscle cells: links to modulation of reactive oxygen species production J. Mol. Endocrinol. 39 1 2007 29 44 (Pubitemid 47337864)
60. W. Barendse, R.J. Bunch, J.W. Kijas, and M.B. Thomas The effect of genetic variation of the retinoic acid receptor-related orphan receptor C gene on fatness in cattle Genetics 175 2 2007 843 853 (Pubitemid 46798281)
61. P. Lau, R.L. Fitzsimmons, S. Raichur, S.C. Wang, A. Lechtken, and G.E. Muscat The orphan nuclear receptor, RORalpha, regulates gene expression that controls lipid metabolism: staggerer (SG/SG) mice are resistant to diet-induced obesity J. Biol. Chem. 283 26 2008 18411 18421
62. C. Chauvet, B. Bois-Joyeux, and J.L. Danan Retinoic acid receptor-related orphan receptor (ROR) alpha4 is the predominant isoform of the nuclear receptor RORalpha in the liver and is up-regulated by hypoxia in HepG2 human hepatoma cells Biochem. J. 364 Pt 2 2002 449 456 (Pubitemid 34620805)
63. D. Zadravec, A. Brolinson, R.M. Fisher, C. Carneheim, R.I. Csikasz, J. Bertrand-Michel, J. Boren, H. Guillou, M. Rudling, and A. Jacobsso Ablation of the very-long-chain fatty acid elongase ELOVL3 in mice leads to constrained lipid storage and resistance to diet-induced obesity FASEB J. 24 11 2010 4366 4377
64. D.J. Peet, S.D. Turley, W. Ma, B.A. Janowski, J.M. Lobaccaro, R.E. Hammer, and D.J. Mangelsdorf Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha Cell 93 5 1998 693 704 (Pubitemid 28257577)
65. N. Vu-Dac, P. Gervois, T. Grotzinger, P. De Vos, K. Schoonjans, J.C. Fruchart, J. Auwerx, J. Mariani, A. Tedgui, and B. Staels Transcriptional regulation of apolipoprotein A-I gene expression by the nuclear receptor RORalpha J. Biol. Chem. 272 36 1997 22401 22404 (Pubitemid 27386046)
66. A. Mamontova, S. Seguret-Mace, B. Esposito, C. Chaniale, M. Bouly, N. Delhaye-Bouchaud, G. Luc, B. Staels, N. Duverger, J. Mariani, and A. Tedgui Severe atherosclerosis and hypoalphalipoproteinemia in the staggerer mouse, a mutant of the nuclear receptor RORalpha Circulation 98 24 1998 2738 2743 (Pubitemid 28564010)
67. E. Raspe, H. Duez, P. Gervois, C. Fievet, J.C. Fruchart, S. Besnard, J. Mariani, A. Tedgui, and B. Staels Transcriptional regulation of apolipoprotein C-III gene expression by the orphan nuclear receptor RORalpha J. Biol. Chem. 276 4 2001 2865 2871
68. I. Duivenvoorden, B. Teusink, P.C. Rensen, J.A. Romijn, L.M. Havekes, and P.J. Voshol Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice Diabetes 54 3 2005 664 671 (Pubitemid 40322068)
69. A. Genoux, H. Dehondt, A. Helleboid-Chapman, C. Duhem, D.W. Hum, G. Martin, L.A. Pennacchio, B. Staels, J. Fruchart-Najib, and J.C. Fruchart Transcriptional regulation of apolipoprotein A5 gene expression by the nuclear receptor RORalpha Arterioscler. Thromb. Vasc. Biol. 25 6 2005 1186 1192 (Pubitemid 40776607)
70. Y. Wang, L.A. Solt, and T.P. Burris Regulation of FGF21 expression and secretion by retinoic acid receptor-related orphan receptor alpha J. Biol. Chem. 285 21 2010 15668 15673
71. J.L. Estall, J.L. Ruas, C.S. Choi, D. Laznik, M. Badman, E. Maratos-Flier, G.I. Shulman, and B.M. Spiegelman PGC-1alpha negatively regulates hepatic FGF21 expression by modulating the heme/Rev-Erb(alpha) axis Proc. Natl. Acad. Sci. U.S.A. 106 52 2009 22510 22515
72. S. Austin, A. Medvedev, Z.H. Yan, H. Adachi, T. Hirose, and A.M. Jetten Induction of the nuclear orphan receptor RORgamma during adipocyte differentiation of D1 and 3T3-L1 cells Cell. Growth Differ. 9 3 1998 267 276 (Pubitemid 28354307)
73. R.L. Sidman, P.W. Lane, and M.M. Dickie Staggerer, a new mutation in the mouse affecting the cerebellum Science 137 1962 610 612
74. R. Bertin, J.M. Guastavino, and R. Portet Effects of cold acclimation on the energetic metabolism of the staggerer mutant mouse Physiol. Behav. 47 2 1990 377 380 (Pubitemid 20098017)
75. T. Meyer, M. Kneissel, J. Mariani, and B. Fournier In vitro and in vivo evidence for orphan nuclear receptor RORalpha function in bone metabolism Proc. Natl. Acad. Sci. U.S.A. 97 16 2000 9197 9202 (Pubitemid 30626697)
76. J.M. Guastavino, R. Bertin, and R. Portet Effects of the rearing temperature on the temporal feeding pattern of the staggerer mutant mouse Physiol. Behav. 49 2 1991 405 409
77. H. Duez, C. Duhem, S. Laitinen, P.S. Patole, M. Abdelkarim, B. Bois-Joyeux, J.L. Danan, and B. Staels Inhibition of adipocyte differentiation by RORalpha FEBS Lett. 583 12 2009 2031 2036
78. N. Ohoka, S. Kato, Y. Takahashi, H. Hayashi, and R. Sato The orphan nuclear receptor RORalpha restrains adipocyte differentiation through a reduction of C/EBPbeta activity and perilipin gene expression Mol. Endocrinol. 23 6 2009 759 771
79. P. Delerive, D. Monte, G. Dubois, F. Trottein, J. Fruchart-Najib, J. Mariani, J.C. Fruchart, and B. Staels The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response EMBO Rep. 2 1 2001 42 48 (Pubitemid 32229720)
80. M. Jaradat, C. Stapleton, S.L. Tilley, D. Dixon, C.J. Erikson, J.G. McCaskill, H.S. Kang, M. Angers, G. Liao, J. Collins, S. Grissom, and A.M. Jetten Modulatory role for retinoid-related orphan receptor alpha in allergen-induced lung inflammation Am. J. Respir. Crit. Care Med. 174 12 2006 1299 1309 (Pubitemid 44913031)
81. B. Kopmels, J. Mariani, N. Delhaye-Bouchaud, F. Audibert, D. Fradelizi, and E.E. Wollman Evidence for a hyperexcitability state of staggerer mutant mice macrophages J. Neurochem. 58 1 1992 192 199
82. J. Bass, and J.S. Takahashi Circadian integration of metabolism and energetics Science 330 6009 2010 1349 1354
83. O. Froy Metabolism and circadian rhythms - implications for obesity Endocr. Rev. 31 1 2010 1 24
84. X. Yang, M. Downes, R.T. Yu, A.L. Bookout, W. He, M. Straume, D.J. Mangelsdorf, and R.M. Evans Nuclear receptor expression links the circadian clock to metabolism Cell 126 4 2006 801 810 (Pubitemid 44233631)
85. M. Akashi, and T. Takumi The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1 Nat. Struct. Mol. Biol. 12 5 2005 441 448 (Pubitemid 43085905)
86. F. Frederic, C. Chianale, C. Oliver, and J. Mariani Enhanced endocrine response to novel environment stress and lack of corticosterone circadian rhythm in staggerer (Rora sg/sg) mutant mice J. Neurosci. Res. 83 8 2006 1525 1532 (Pubitemid 43844997)
87. T.K. Sato, S. Panda, L.J. Miraglia, T.M. Reyes, R.D. Rudic, P. McNamara, K.A. Naik, G.A. FitzGerald, S.A. Kay, and J.B. Hogenesch A functional genomics strategy reveals Rora as a component of the mammalian circadian clock Neuron 43 4 2004 527 537 (Pubitemid 39094679)
88. N. Preitner, F. Damiola, L. Lopez-Molina, J. Zakany, D. Duboule, U. Albrecht, and U. Schibler The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator Cell 110 2 2002 251 260 (Pubitemid 34876552)
89. C. Crumbley, Y. Wang, D.J. Kojetin, and T.P. Burris Characterization of the core mammalian clock component, NPAS2, as a REV-ERB{alpha}/ROR{alpha} target gene J. Biol. Chem. 2010
90. G. Le Martelot, T. Claudel, D. Gatfield, O. Schaad, B. Kornmann, G.L. Sasso, A. Moschetta, and U. Schibler REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis PLoS Biol. 7 9 2009 e1000181
91. D. Feng, T. Liu, Z. Sun, A. Bugge, S.E. Mullican, T. Alenghat, X.S. Liu, and M.A. Lazar A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism Science 331 6022 2011 1315 1319
92. A.M. Jetten Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism Nucl. Recept. Signal. 7 2009 e003
93. E. Trenkner, and M.K. Hoffmann Defective development of the thymus and immunological abnormalities in the neurological mouse mutation "staggerer" J. Neurosci. 6 6 1986 1733 1737 (Pubitemid 16078348)
94. P.M. Ridker, N. Rifai, N.R. Cook, G. Bradwin, and J.E. Buring Non-HDL cholesterol, apolipoproteins A-I and B100, standard lipid measures, lipid ratios, and CRP as risk factors for cardiovascular disease in women JAMA 294 3 2005 326 333 (Pubitemid 41043776)
95. J. Frostegard Atherosclerosis in patients with autoimmune disorders Arterioscler. Thromb. Vasc. Biol. 25 9 2005 1776 1785 (Pubitemid 41243443)
96. S. Besnard, C. Heymes, R. Merval, M. Rodriguez, J.P. Galizzi, J.A. Boutin, J. Mariani, and A. Tedgui Expression and regulation of the nuclear receptor RORalpha in human vascular cells FEBS Lett. 511 1-3 2002 36 40 (Pubitemid 34127819)
97. S. Besnard, J.S. Silvestre, M. Duriez, J. Bakouche, Y. Lemaigre-Dubreuil, J. Mariani, B.I. Levy, and A. Tedgui Increased ischemia-induced angiogenesis in the staggerer mouse, a mutant of the nuclear receptor Roralpha Circ. Res. 89 12 2001 1209 1215 (Pubitemid 34627880)
98. C.M Stapleton, M. Jaradat, D. Dixon, H.S. Kang, S.C. Kim, G. Liao, M.A. Carey, J. Cristiano, M.P. Moorman, and A.M. Jetten Enhanced susceptibility of staggerer (RORalphasg/sg) mice to lipopolysaccharide-induced lung inflammation Am. J. Physiol. Lung Cell. Mol. Physiol. 289 1 2005 L1144
99. J.M. Lee, I.S. Kim, H. Kim, J.S. Lee, K. Kim, H.Y. Yim, J. Jeong, J.H. Kim, J.Y. Kim, H. Lee, S.B. Seo, M.G. Rosenfeld, K.I. Kim, and S.H. Baek RORalpha attenuates Wnt/beta-catenin signaling by PKCalpha-dependent phosphorylation in colon cancer Mol. Cell. 37 2 2010 183 195
100. S.J. George Wnt pathway: a new role in regulation of inflammation Arterioscler. Thromb. Vasc. Biol. 28 3 2008 400 402
101. N. Ouchi, A. Higuchi, K. Ohashi, Y. Oshima, N. Gokce, R. Shibata, Y. Akasaki, A. Shimono, and K. Walsh Sfrp5 is an anti-inflammatory adipokine that modulates metabolic dysfunction in obesity Science 329 5990 2010 454 457
102. S.E. Ross, N. Hemati, K.A. Longo, C.N. Bennett, P.C. Lucas, R.L. Erickson, and O.A. MacDougald Inhibition of adipogenesis by Wnt signaling Science 289 5481 2000 950 953 (Pubitemid 30659947)
103. J.M. Guastavino Constraint of the mother with pups restores some aspects of the maternal behavior of mutant staggerer mice Physiol. Behav. 30 5 1983 771 774 (Pubitemid 13058955)
104. H.S. Kang, K. Okamoto, Y. Takeda, J.Y. Beak, K.E. Gerrish, C.D. Bortner, L.M. Degraff, T. Wada, W. Xie, and A.M. Jetten Transcriptional profiling reveals a role for ROR{alpha} in regulating gene expression in obesity-associated inflammation and hepatic steatosis Physiol. Genomics 2011