The orphan nuclear receptor RORα restrains adipocyte differentiation through a reduction of C/EBPβ activity and perilipin gene expression

Molecular Endocrinology

Volumn 23, Issue 6, 2009, Pages 759-771

  Ohoka, Nobumichi ^a,b   Kato, Shogo ^a   Takahashi, Yu ^a   Hayashi, Hidetoshi ^c   Sato, Ryuichiro ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b Basic Research Activities for Innovative Biosciences   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; CELL NUCLEUS RECEPTOR; FAT DROPLET; PERILIPIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN P300; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR RELATED ORPHAN RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; TRANSCRIPTION INITIATION;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CHROMATIN; DNA; E1A-ASSOCIATED P300 PROTEIN; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MICE; PHOSPHOPROTEINS; PHOSPHORYLATION; PPAR GAMMA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 66449122523     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0277     Document Type: Article

References (62)

1. Spiegelman BM, Flier JS 2001 Obesity and the regulation of energy balance. Cell 104:531-543
2. Farmer SR 2006 Transcriptional control of adipocyte formation. Cell Metab 4:263-273
3. Rosen ED, MacDougald OA 2006 Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885-896
4. Green H, Kehinde O 1979 Formation of normally differentiated subcutaneous fat pads by an established preadipose cell line. J Cell Physiol 101:169-171
5. Green H, Meuth M 1974 An established pre-adipose cell line and its differentiation in culture. Cell 3:127-133
6. Darlington GJ, Ross SE, MacDougald OA 1998 The role of C/EBP genes in adipocyte differentiation. J Biol Chem 273:30057-30060
7. Tontonoz P, Hu E, Spiegelman BM 1994 Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell 79:1147-1156
8. Rubin CS, Hirsch A, Fung C, Rosen OM 1978 Development of hormone receptors and hormonal responsiveness in vitro. Insulin receptors and insulin sensitivity in the preadipocyte and adipocyte forms of 3T3-L1 cells. J Biol Chem 253:7570-7578
9. Cao Z, Umek RM, McKnight SL 1991 Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 5:1538-1552
10. Green H, Kehinde O 1975 An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5:19-27
11. Wiper-Bergeron N, Wu D, Pope L, Schild-Poulter C, Hacheé RJ 2003 Stimulation of preadipocyte differentiation by steroid through targeting of an HDAC1 complex. EMBO J 22:2135-2145
12. Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, McKeon C, Darlington GJ, Spiegelman BM 1999 Cross-regulation of C/EBPα and PPARγ controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 3:151-158
13. Freytag SO, Paielli DL, Gilbert JD 1994 Ectopic expression of the CCAAT/enhancer-binding protein α promotes the adipogenic program in a variety of mouse fibroblastic cells. Genes Dev 8:1654-1663
14. Rosen ED, Sarraf P, Troy AE, Bradwin G, Moore K, Milstone DS, Spiegelman BM, Mortensen RM 1999 PPARγ is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell 4:611-617
15. Arimura N, Horiba T, Imagawa M, Shimizu M, Sato R 2004 The peroxisome proliferator-activated receptor γ regulates expression of the perilipin gene in adipocytes. J Biol Chem 279:10070-10076
16. Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, Gonzalez FJ, Spiegelman BM 2002 C/EBPα induces adipogenesis through PPARγ: a unified pathway. Genes Dev 16:22-26
17. Kim JB, Sarraf P, Wright M, Yao KM, Mueller E, Solanes G, Lowell BB, Spiegelman BM 1998 Nutritional and insulin regulation of fatty acid synthetase and leptin gene expression through ADD1/SREBP1. J Clin Invest 101:1-9
18. Fajas L, Schoonjans K, Gelman L, Kim JB, Najib J, Martin G, Fruchart JC, Briggs M, Spiegelman BM, Auwerx J 1999 Regulation of peroxisome proliferator-activated receptor γ expression by adipocyte differentiation and determination factor 1/sterol regulatory element binding protein 1: implications for adipocyte differentiation and metabolism. Mol Cell Biol 19:5495-5503
19. Kim JB, Wright HM, Wright M, Spiegelman BM 1998 ADD1/SREBP1 activates PPARγ through the production of endogenous ligand. Proc Natl Acad Sci USA 95:4333-4337
20. Yeh WC, Cao Z, Classon M, McKnight SL 1995 Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev 9:168-181
21. Tanaka T, Yoshida N, Kishimoto T, Akira S 1997 Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBPδ gene. EMBO J 16:7432-7443
22. Tang QQ, Otto TC, Lane MD 2003 CCAAT/enhancer-binding protein β is required for mitotic clonal expansion during adipogenesis. Proc Natl Acad Sci USA 100:850-855
23. MacDougald OA, Mandrup S 2002 Adipogenesis: forces that tip the scales. Trends Endocrinol Metab 13:5-11
24. Pedersen SB, Bruun JM, Hube F, Kristensen K, Hauner H, Richelsen B 2001 Demonstration of estrogen receptor subtypes α and β in human adipose tissue: influences of adipose cell differentiation and fat depot localization. Mol Cell Endocrinol 182:27-37
25. Boukhtouche F, Mariani J, Tedgui A 2004 The "CholesteROR" protective pathway in the vascular system. Arterioscler Thromb Vasc Biol 24:637-643
26. Dzhagalov I, Zhang N, He YW 2004 The roles of orphan nuclear receptors in the development and function of the immune system. Cell Mol Immunol 1:401-407
27. Takahashi Y, Ohoka N, Hayashi H, Sato R 2008 TRB3 suppresses adipocyte differentiation by negatively regulating PPARγ transcriptional activity. J Lipid Res 49:880-892
28. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H 2005 TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24:1243-1255
29. Miyata Y, Fukuhara A, Matsuda M, Komuro R, Shimomura I 2008 Insulin induces chaperone and CHOP gene expressions in adipocytes. Biochem Biophys Res Commun 365:826-832
30. Bezy O, Vernochet C, Gesta S, Farmer SR, Kahn CR 2007 TRB3 blocks adipocyte differentiation through the inhibition of C/EBPβ transcriptional activity. Mol Cell Biol 27:6818-6831
31. Ding J, Kato S, Du K 2008 PI3K activates negative and positive signals to regulate TRB3 expression in hepatic cells. Exp Cell Res 314:1566-1574
32. Baer M, Johnson PF 2000 Generation of truncated C/EBPβ isoforms by in vitro proteolysis. J Biol Chem 275:26582-26590
33. Welm AL, Timchenko NA, Darlington GJ 1999 C/EBPα regulates generation of C/EBPβ isoforms through activation of specific proteolytic cleavage. Mol Cell Biol 19:1695-1704
34. Tang QQ, Grønborg M, Huang H, Kim JW, Otto TC, Pandey A, Lane MD 2005 Sequential phosphorylation of CCAAT enhancer-binding protein β by MAPK and glycogen synthase kinase 3β is required for adipogenesis. Proc Natl Acad Sci USA 102:9766-9771
35. Zuo Y, Qiang L, Farmer SR 2006 Activation of CCAAT/enhancer-binding protein (C/EBP) α expression by C/EBPβ during adipogenesis requires a peroxisome proliferator-activated receptor-γ-associated repression of HDAC1 at the C/EBPα gene promoter. J Biol Chem 281:7960-7967
36. Giguère V, Tini M, Flock G, Ong ES, Evans RM, Otulakowski G 1994 Isoform-specific amino-terminal domains dictate DNA-binding properties of RORα, a novel family of orphan hormone nuclear receptors. Genes Dev 8:538-553
37. Giguère V, McBroom LD, Flock G 1995 Determinants of target gene specificity for RORα1: monomeric DNA binding by an orphan nuclear receptor. Mol Cell Biol 15:2517-2526
38. Martinez-Botas J, Anderson JB, Tessier D, Lapillonne A, Chang BH, Quast MJ, Gorenstein D, Chen KH, Chan L 2000 Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat Genet 26:474-479
39. Brasaemle DL, Rubin B, Harten IA, Gruia-Gray J, Kimmel AR, Londos C 2000 Perilipin A increases triacylglycerol storage by decreasing the rate of triacylglycerol hydrolysis. J Biol Chem 275:38486-38493
40. Tansey JT, Sztalryd C, Gruia-Gray J, Roush DL, Zee JV, Gavrilova O, Reitman ML, Deng CX, Li C, Kimmel AR, Londos C 2001 Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc Natl Acad Sci USA 98:6494-6499
41. Naiki T, Saijou E, Miyaoka Y, Sekine K, Miyajima A 2007 TRB2, a mouse Tribbles ortholog, suppresses adipocyte differentiation by inhibiting AKT and C/EBPβ. J Biol Chem 282:24075-24082
42. Cui TX, Piwien-Pilipuk G, Huo JS, Kaplani J, Kowk R, Schwartz J 2005 Endogenous CCAAT/enhancer binding protein β and p300 are both regulated by growth hormone to mediate transcriptional activation. Mol Endocrinol 19:2175-2186
43. Wiper-Bergeron N, Salem HA, Tomlinson JJ, Wu D, Haché RJ 2007 Glucocorticoid-stimulated preadipocyte differentiation is mediated through acetylation of C/EBPβ by GCN5. Proc Natl Acad Sci USA 104:2703-2708
44. Forman BM, Chen J, Blumberg B, Kliewer SA, Henshaw R, Ong ES, Evans RM 1994 Cross-talk among RORα1 and the Rev-erb family of orphan nuclear receptors. Mol Endocrinol 8:1253-1261
45. Delerive P, Chin WW, Suen CS 2002 Identification of Reverbα as a novel RORα target gene. J Biol Chem 277:35013-35018
46. Raspè E, Mautino G, Duval C, Fontaine C, Duez H, Barbier O, Monte D, Fruchart J, Fruchart J, Staels B 2002 Transcriptional regulation of human Rev-erbα gene expression by the orphan nuclear receptor retinoic acid-related orphan receptor α. J Biol Chem 277:49275-49281
47. Fontaine C, Dubois G, Duguay Y, Helledie T, Vu-Dac N, Gervois P, Soncin F, Mandrup S, Fruchart JC, Fruchar-Najib J, Staels B 2003 The orphan nuclear receptor Rev-Erbα is a peroxisome proliferator-activated receptor (PPAR) γ target gene and promotes PPARγ-induced adipocyte differentiation. J Biol Chem 278:37672-37680
48. Shimba S, Ishii N, Ohta Y, Ohno T, Watabe Y, Hayashi M, Wada T, Aoyagi T, Tezuka M 2005 Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci USA 102:12071-12706
49. Miki N, Ikuta M, Matsui T 2004 Hypoxia-induced activation of the retinoic acid receptor-related orphan receptor α4 gene by an interaction between hypoxia-inducible factor-1 and Sp1. J Biol Chem 279:15025-15031
50. Boukhtouche F, Doulazmi M, Frederic F, Dusart I, Brugg B, Mariani J 2006 RORα, a pivotal nuclear receptor for Purkinje neuron survival and differentiation: from development to ageing. Cerebellum 5:97-104
51. Lau P, Bailey P, Dowhan DH, Muscat GE 1999 Exogenous expression of a dominant negative RORα1 vector in muscle cells impairs differentiation: RORα1 directly interacts with p300 and myoD. Nucleic Acids Res 27:411-420
52. Jarvis CI, Staels B, Brugg B, Lemaigre-Dubreuil Y, Tedgui A, Mariani J 2002 Age-related phenotypes in the staggerer mouse expand the RORα nuclear receptor's role beyond the cerebellum. Mol Cell Endocrinol 186:1-5
53. Lau P, Fitzsimmons RL, Raichur S, Wang SC, Lechtken A, Muscat GE 2008 The orphan nuclear receptor, RORα, regulates gene expression that controls lipid metabolism: staggerer (SG/SG) mice are resistant to diet-induced obesity. J Biol Chem 283:18411-18421
54. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, Furukawa S, Tochino Y, Komuro R, Matsuda M, Shimomura I 2007 Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56:901-911
55. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Görgün C, Glimcher LH, Hotamisligil GS 2004 Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461
56. Lau DC, Dhillon B, Yan H, Szmitko PE, Verma S 2005 Adipokines: molecular links between obesity and atherosclerosis. Am J Physiol Heart Circ Physiol 288:H2031-H2041
57. Guzik TJ, Mangalat D, Korbut R 2006 Adipocytokines: novel link between inflammation and vascular function? J Physiol Pharmacol 57:505-528
58. Chauvet C, Bois-Joyeux B, Berra E, Pouyssegur J, Danan JL 2004 The gene encoding human retinoic acid-receptor-related orphan receptor α is a target for hypoxia-inducible factor 1. Biochem J 384:79-85
59. Ohoka N, Hattori T, Kitagawa M, Onozaki K, Hayashi H 2007 Critical and functional regulation of CHOP (C/EBP homologous protein) through the N-terminal portion. J Biol Chem 282:35687-35694
60. Akashi M, Takumi T 2005 The orphan nuclear receptor RORα regulates circadian transcription of the mammalian core-clock Bmal1. Nat Struct Mol Biol 12:441-448
61. Descombes P, Schibler U 1991 A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67:569-579
62. Hattori T, Ohoka N, Inoue Y, Hayashi H, Onozaki K 2003 C/EBP family transcription factors are degraded by the proteasome but stabilized by forming dimer. Oncogene 22:1273-1280