Transient expression of interferon-inducible p204 in the early stage is required for adipogenesis in 3T3-L1 cells

Endocrinology

Volumn 151, Issue 7, 2010, Pages 3141-3153

  Xiao, Jing ^a   Sun, Bing ^b   Cai, Guo Ping ^a  

^a TSINGHUA UNIVERSITY   (China)

^b INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPSIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; LIPOPROTEIN LIPASE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; PROTEIN P204; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CCAAT ENHANCER BINDING PROTEIN DELTA; COMPLEMENT FACTOR D; IFI16 PROTEIN, MOUSE; NUCLEAR PROTEIN; PHOSPHOPROTEIN;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EXPRESSION VECTOR; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ADIPOSE TISSUE; ANIMAL; CELL STRAIN 3T3; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; MOUSE; NUDE MOUSE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

3T3-L1 CELLS; ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; COMPLEMENT FACTOR D; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOPRECIPITATION; LIPOPROTEIN LIPASE; MICE; MICE, NUDE; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PPAR GAMMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 77954596880     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1381     Document Type: Article

References (63)

1. Opdenakker G, Snoddy J, Choubey D, Toniato E, Pravtcheva DD, Seldin MF, Ruddle FH, Lengyel P 1989 Interferons as gene activators: a cluster of six interferon-activatable genes is linked to the erythroid α-spectrin locus on murine chromosome 1. Virology 171:568-578
2. Choubey D, Li SJ, Datta B, Gutterman JU, Lengyel P 1996 Inhibition of E2F-mediated transcription by p202.EMBOJ 15:5668-5678
3. Lembo M, Sacchi C, Zappador C, Bellomo G, Gaboli M, Pandolfi PP, Gariglio M, Landolfo S 1998 Inhibition of cell proliferation by the interferon-inducible 204 gene, a member of the Ifi 200 cluster. Oncogene 16:1543-1551
4. Liu CJ, Wang H, Lengyel P 1999 The interferon-inducible nucleolar p204 protein binds the ribosomal RNA-specific UBF1 transcription factor and inhibits ribosomal RNA transcription. EMBO J 18:2845-2854
5. Min W, Ghosh S, Lengyel P 1996 The interferon-inducible p202 protein as a modulator of transcription: inhibition of NF-κB, c-Fos, and c-Jun activities. Mol Cell Biol 16:359-368
6. Xin H, D'Souza S, Fang L, Lengyel P, Choubey D 2001 p202, an interferon-inducible negative regulator of cell growth, is a target of the adenovirus E1A protein. Oncogene 20:6828-6839
7. Datta B, Min W, Burma S, Lengyel P 1998 Increase in p202 expression during skeletal muscle differentiation: inhibition of MyoD protein expression and activity by p202. Mol Cell Biol 18:1074-1083
8. Dauffy J, Mouchiroud G, Bourette RP 2006 The interferon-inducible gene, Ifi204, is transcriptionally activated in response to M-CSF, and its expression favors macrophage differentiation in myeloid progenitor cells. J Leukoc Biol 79:173-183
9. Ding B, Liu CJ, Huang Y, Hickey RP, Yu J, Kong W, Lengyel P 2006 p204 is required for the differentiation of P19 murine embryonal carcinoma cells to beating cardiac myocytes: its expression is activated by the cardiac Gata4, Nkx2.5, and Tbx5 proteins. J Biol Chem 281:14882-14892
10. Ding B, Liu CJ, Huang Y, Yu J, Kong W, Lengyel P 2006 p204 protein overcomes the inhibition of the differentiation of P19 murine embryonal carcinoma cells to beating cardiac myocytes by Id proteins. J Biol Chem 281:14893-14906
11. Geng Y, Choubey D 2000 Differential induction of the 200-family proteins in Daudi Burkitt's lymphoma cells by interferon-α. J Biol Regul Homeost Agents 14:263-268
12. Kong L, Liu CJ 2008 Mediation of chondrogenic and osteogenic differentiation by an interferon-inducible p202 protein. Cell Mol Life Sci 65:3494-3506
13. Liu C, Wang H, Zhao Z, Yu S, Lu YB, Meyer J, Chatterjee G, Deschamps S, Roe BA, Lengyel P 2000 MyoD-dependent induction during myoblast differentiation of p204, a protein also inducible by interferon. Mol Cell Biol 20:7024-7036
14. Liu CJ, Chang E, Yu J, Carlson CS, Prazak L, Yu XP, Ding B, Lengyel P, Di Cesare PE 2005 The interferon-inducible p204 protein acts as a transcriptional coactivator of Cbfa1 and enhances osteoblast differentiation. J Biol Chem 280:2788-2796
15. Liu CJ, Ding B, Wang H, Lengyel P 2002 The MyoD-inducible p204 protein overcomes the inhibition of myoblast differentiation by Id proteins. Mol Cell Biol 22:2893-2905
16. Luan Y, Yu XP, Xu K, Ding B, Yu J, Huang Y, Yang N, Lengyel P, Di Cesare PE, Liu CJ 2007 The retinoblastoma protein is an essential mediator of osteogenesis that links the p204 protein to the Cbfa1 transcription factor thereby increasing its activity. J Biol Chem 282:16860-16870
17. Luan Y, Yu XP, Yang N, Frenkel S, Chen L, Liu CJ 2008 p204 protein overcomes the inhibition of core binding factor α-1-mediated osteogenic differentiation by Id helix-loop-helix proteins. Mol Biol Cell 19:2113-2126
18. Zhang Y, Kong L, Carlson CS, Liu CJ 2008 Cbfa1-dependent expression of an interferon-inducible p204 protein is required for chondrocyte differentiation. Cell Death Differ 15:1760-1771
19. Zhang Y, Tian Q, Du Y, Cao H, Lengyel P, Kong W 2008 Multiple splicing results in at least two p203 proteins that are expressed in the liver and down-regulated during liver regeneration. Front Biosci 13:2444-2451
20. Aglipay JA, Lee SW, Okada S, Fujiuchi N, Ohtsuka T, Kwak JC, Wang Y, Johnstone RW, Deng C, Qin J, Ouchi T 2003 A member of the Pyrin family, IFI16, is a novel BRCA1-associated protein involved in the p53-mediated apoptosis pathway. Oncogene 22:8931-8938
21. Wang H, Liu C, Lu Y, Chatterjee G, Ma XY, Eisenman RN, Lengyel P 2000 The interferon- and differentiation-inducible p202a protein inhibits the transcriptional activity of c-Myc by blocking its association with Max. J Biol Chem 275:27377-27385
22. Xin H, D'Souza S, Jørgensen TN, Vaughan AT, Lengyel P, Kotzin BL, Choubey D 2006 Increased expression of Ifi202, an IFN-activatable gene, in B6.Nba2 lupus susceptible mice inhibits p53-mediated apoptosis. J Immunol 176:5863-5870
23. Rolle S, De Andrea M, Gioia D, Lembo D, Hertel L, Landolfo S, Gariglio M 2001 The interferon-inducible 204 gene is transcriptionally activated by mouse cytomegalovirus and is required for its replication. Virology 286:249-255
24. Xin H, Pereira-Smith OM, Choubey D 2004 Role of IFI 16 in cellular senescence of human fibroblasts. Oncogene 23:6209-6217
25. D'Souza S, Xin H, Walter S, Choubey D 2001 The gene encoding p202, an interferon-inducible negative regulator of the p53 tumor suppressor, is a target of p53-mediated transcriptional repression. J Biol Chem 276:298-305
26. Dermott JM, Gooya JM, Asefa B, Weiler SR, Smith M, Keller JR 2004 Inhibition of growth by p205: a nuclear protein and putative tumor suppressor expressed during myeloid cell differentiation. Stem Cells 22:832-848
27. Johnstone RW, Wei W, Greenway A, Trapani JA 2000 Functional interaction between p53 and the interferon-inducible nucleoprotein IFI 16. Oncogene 19:6033-6042
28. Yan DH, Wen Y, Spohn B, Choubey D, Gutterman JU, Hung MC 1999 Reduced growth rate and transformation phenotype of the prostate cancer cells by an interferon-inducible protein, p202. Oncogene 18:807-811
29. Cornelius P, MacDougald OA, Lane MD 1994 Regulation of adipocyte development. Annu Rev Nutr 14:99-129
30. De Andrea M, Zannetti C, Noris E, Gariglio M, Azzimonti B, Landolfo S 2002 The mouse interferon-inducible gene Ifi204 product interacts with the Tpr protein, a component of the nuclear pore complex. J Interferon Cytokine Res 22:1113-1121
31. Ding B, Lengyel P 2008 p204 protein is a novel modulator of ras activity. J Biol Chem 283:5831-5848
32. Gregoire FM, Smas CM, Sul HS 1998 Understanding adipocyte differentiation. Physiol Rev 78:783-809
33. Ericsson J, Jackson SM, Kim JB, Spiegelman BM, Edwards PA 1997 Identification of glycerol-3-phosphate acyltransferase as an adipocyte determination and differentiation factor 1- and sterol regulatory element-binding protein-responsive gene. J Biol Chem 272:7298-7305
34. Lane MD, Tang QQ, Jiang MS 1999 Role of the CCAAT enhancer binding proteins (C/EBPs) in adipocyte differentiation. Biochem Biophys Res Commun 266:677-683
35. 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
36. 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
37. Christy RJ, Kaestner KH, Geiman DE, Lane MD 1991 CCAAT/enhancer binding protein gene promoter: binding of nuclear factors during differentiation of 3T3-L1 preadipocytes. Proc Natl Acad Sci USA 88:2593-2597
38. Clarke SL, Robinson CE, Gimble JM 1997 CAAT/enhancer binding proteins directly modulate transcription from the peroxisome proliferator-activated receptor γ 2 promoter. Biochem Biophys Res Commun 240:99-103
39. Shao D, Lazar MA 1997 Peroxisome proliferator activated receptor γ, CCAAT/enhancer-binding protein α, and cell cycle status regulate the commitment to adipocyte differentiation. J Biol Chem 272:21473-21478
40. Mizuno H 2009 Adipose-derived stem cells for tissue repair and regeneration: ten years of research and a literature review. J Nippon Med Sch 76:56-66
41. Ikeda D, Sakaue S, Kamigaki M, Ohira H, Itoh N, Ohtsuka Y, Tsujino I, Nishimura M 2008 Knockdown of macrophage migration inhibitory factor disrupts adipogenesis in 3T3-L1 cells. Endocrinology 149:6037-6042
42. Shimabukuro M, Koyama K, Chen G, Wang MY, Trieu F, Lee Y, Newgard CB, Unger RH 1997 Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Natl Acad Sci USA 94:4637-4641
43. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M 2000 Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852
44. 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/ebp α gene promoter. J Biol Chem 281:7960-7967
45. Shibasaki M, Takahashi K, Itou T, Miyazawa S, Ito M, Kobayashi J, Bujo H, Saito Y 2002 Alterations of insulin sensitivity by the implantation of 3T3-L1 cells in nude mice. A role for TNF-α? Diabetologia 45:518-526
46. Choubey D, Lengyel P 1992 Interferon action: nucleolar and nucleoplasmic localization of the interferon-inducible 72-kD protein that is encoded by the Ifi 204 gene from the gene 200 cluster. J Cell Biol 116:1333-1341
47. Choubey D, Snoddy J, Chaturvedi V, Toniato E, Opdenakker G, Thakur A, Samanta H, Engel DA, Lengyel P 1989 Interferons as gene activators. Indications for repeated gene duplication during the evolution of a cluster of interferon-activatable genes on murine chromosome 1. J Biol Chem 264:17182-17189
48. de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BR 2001 Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol 69:912-920
49. Landolfo S, Gribaudo G, Angeretti A, Gariglio M 1995 Mechanisms of viral inhibition by interferons. Pharmacol Ther 65:415-442
50. Luan Y, Lengyel P, Liu CJ 2008 p204, A p200 family protein, as a multifunctional regulator of cell proliferation and differentiation. Cytokine Growth Factor Rev 19:357-369
51. Tang QQ, Otto TC, Lane MD 2003 Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc Natl Acad Sci USA 100:44-49
52. Moldes M, Boizard M, Liepvre XL, Feve B, Dugail I, Pairault J 1999 Functional antagonism between inhibitor of DNA binding (Id) and adipocyte determination and differentiation factor 1/sterol regulatory element-binding protein-1c (ADD1/SREBP-1c) trans-factors for the regulation of fatty acid synthase promoter in adipocytes. Biochem J 344(Pt 3):873-880
53. Lin FT, Lane MD 1994 CCAAT/enhancer binding protein α is sufficient to initiate the 3T3-L1 adipocyte differentiation program. Proc Natl Acad Sci USA 91:8757-8761
54. Puigserver P, Ribot J, Serra F, Gianotti M, Bonet ML, Nadal-Ginard B, Palou A 1998 Involvement of the retinoblastoma protein in brown and white adipocyte cell differentiation: functional and physical association with the adipogenic transcription factor C/EBPα. Eur J Cell Biol 77:117-123
55. Nishimura S, Manabe I, Nagasaki M, Hosoya Y, Yamashita H, Fujita H, Ohsugi M, Tobe K, Kadowaki T, Nagai R, Sugiura S 2007 Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels. Diabetes 56:1517-1526
56. Liu B, Faia L, Hu M, Nussenblatt RB 2010 Pro-angiogenic effect of IFNγ is dependent on the PI3K/mTOR/translational pathway in human retinal pigmented epithelial cells. Mol Vis 16:184-193
57. Indraccolo S 2010 Interferon-α as angiogenesis inhibitor: learning from tumor models. Autoimmunity 43:244-247
58. Dauffy J, Mouchiroud G, Bourette RP 2006 The interferon-inducible gene, Ifi204, is transcriptionally activated in response to M-CSF, and its expression favors macrophage differentiation in myeloid progenitor cells. J Leukoc Biol 79:173-183
59. Bourette RP, Mouchiroud G 2008 The biological role of interferon-inducible P204 protein in the development of the mononuclear phagocyte system. Front Biosci 13:879-886
60. Wang H, Ding B, Liu CJ, Ma XY, Deschamps S, Roe BA, Lengyel P 2002 The increase in levels of interferon-inducible proteins p202a and p202b and RNA-dependent protein kinase (PKR) during myoblast differentiation is due to transactivation by MyoD: their tissue distribution in uninfected mice does not depend on interferons. J Interferon Cytokine Res 22:729-737
61. Welch JS, Ricote M, Akiyama TE, Gonzalez FJ, Glass CK 2003 PPARγ and PPARδ negatively regulate specific subsets of lipopolysaccharide and IFN-γ target genes in macrophages. Proc Natl Acad Sci USA 100:6712-6717
62. Hertel L, Rolle S, De Andrea M, Azzimonti B, Osello R, Gribaudo G, Gariglio M, Landolfo S 2000 The retinoblastoma protein is an essential mediator that links the interferon-inducible 204 gene to cell-cycle regulation. Oncogene 19:3598-3608
63. Lengyel P 2008 From RNase L to the multitalented p200 family proteins: an exploration of the modes of interferon action. J Interferon Cytokine Res 28:273-281