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PMID: 15985551 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis.

Tang QQ, Grønborg M, Huang H, Kim JW, Otto TC, Pandey A, Lane MD

Abstract

CCAAT enhancer-binding protein (C/EBP)beta, C/EBPalpha, and peroxisome proliferator activated receptor (PPAR)gamma act in a cascade where C/EBPbeta activates expression of C/EBPalpha and PPARgamma, which then function as pleiotropic activators of genes that produce the adipocyte phenotype. When growth-arrested 3T3-L1 preadipocytes are induced to differentiate, C/EBPbeta is rapidly expressed but still lacks DNA-binding activity. After a long (14-hour) lag, glycogen synthase kinase 3beta enters the nucleus, which correlates with hyperphosphorylation of C/EBPbeta and acquisition of DNA-binding activity. Concurrently, 3T3-L1 preadipocytes synchronously enter S phase and undergo mitotic clonal expansion, a prerequisite for terminal differentiation. Ex vivo and in vitro experiments with C/EBPbeta show that phosphorylation of Thr-188 by mitogen-activating protein kinase "primes" C/EBPbeta for subsequent phosphorylation on Ser-184 and Thr-179 by glycogen synthase kinase 3beta, acquisition of DNA-binding function, and transactivation of the C/EBPalpha and PPARgamma genes. The delayed transactivation of the C/EBPalpha and PPARgamma genes by C/EBPbeta appears necessary to allow mitotic clonal expansion, which would otherwise be prevented, because C/EBPalpha and PPARgamma are antimitotic.

MeSH Terms
3T3-L1 Cells Adipocytes/cytology,metabolism Animals CCAAT-Enhancer-Binding Protein-beta/metabolism Cell Differentiation/physiology Cell Nucleus/metabolism Chromatin Immunoprecipitation Chromatography, Liquid Electrophoresis, Polyacrylamide Gel Glycogen Synthase Kinase 3/metabolism Glycogen Synthase Kinase 3 beta Immunoblotting Isoelectric Focusing Mass Spectrometry Mice Mitogen-Activated Protein Kinases/metabolism PPAR gamma/metabolism Phosphorylation Transcriptional Activation/physiology
Chemicals
CCAAT-Enhancer-Binding Protein-beta PPAR gamma Glycogen Synthase Kinase 3 beta Gsk3b protein, mouse Mitogen-Activated Protein Kinases Glycogen Synthase Kinase 3
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Tang Qi-Qun
Departments of Pediatrics (Division of Endocrinology), McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. qtang1@jhem.jhmi.edu
Grønborg Mads
Huang Haiyan
Kim Jae-Woo
Otto Tamara C
Pandey Akhilesh
Lane M Daniel
References (30)
30 references, click to expand
  1. Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes.
    J Biol Chem. 1980 May 25;255(10):4745-50 PMID: 7372608
  2. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  3. CCAAT/enhancer-binding protein alpha (C/EBP alpha) inhibits cell proliferation through the p21 (WAF-1/CIP-1/SDI-1) protein.
    Genes Dev. 1996 Apr 1;10(7):804-15 PMID: 8846917
  4. The organization, promoter analysis, and expression of the human PPARgamma gene.
    J Biol Chem. 1997 Jul 25;272(30):18779-89 PMID: 9228052
  5. CCAAT/enhancer binding protein alpha regulates p21 protein and hepatocyte proliferation in newborn mice.
    Mol Cell Biol. 1997 Dec;17(12):7353-61 PMID: 9372966
  6. Repressive effect of Sp1 on the C/EBPalpha gene promoter: role in adipocyte differentiation.
    Mol Cell Biol. 1999 Jul;19(7):4855-65 PMID: 10373535
  7. Activation and centromeric localization of CCAAT/enhancer-binding proteins during the mitotic clonal expansion of adipocyte differentiation.
    Genes Dev. 1999 Sep 1;13(17):2231-41 PMID: 10485846
  8. CCAAT-enhancer binding protein: a component of a differentiation switch.
    Science. 1991 Jan 18;251(4991):288-92 PMID: 1987644
  9. CCAAT/enhancer binding protein gene promoter: binding of nuclear factors during differentiation of 3T3-L1 preadipocytes.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2593-7 PMID: 2006196
  10. Cell-free transcription directed by the 422 adipose P2 gene promoter: activation by the CCAAT/enhancer binding protein.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8465-9 PMID: 1681537
  11. Calcium-regulated phosphorylation within the leucine zipper of C/EBP beta.
    Science. 1992 Apr 17;256(5055):370-3 PMID: 1314426
  12. Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2207-11 PMID: 8384717
  13. Circadian transcription of the cholesterol 7 alpha hydroxylase gene may involve the liver-enriched bZIP protein DBP.
    Genes Dev. 1993 Oct;7(10):1871-84 PMID: 8405996
  14. A 30-kDa alternative translation product of the CCAAT/enhancer binding protein alpha message: transcriptional activator lacking antimitotic activity.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9606-10 PMID: 8415748
  15. Protein kinase A and C site-specific phosphorylations of LAP (NF-IL6) modulate its binding affinity to DNA recognition elements.
    J Clin Invest. 1994 Jun;93(6):2554-61 PMID: 8200992
  16. CRP2 (C/EBP beta) contains a bipartite regulatory domain that controls transcriptional activation, DNA binding and cell specificity.
    EMBO J. 1995 Jul 3;14(13):3170-83 PMID: 7621830
  17. Structural organization of mouse peroxisome proliferator-activated receptor gamma (mPPAR gamma) gene: alternative promoter use and different splicing yield two mPPAR gamma isoforms.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7921-5 PMID: 7644514
  18. Transcriptional regulation of gene expression during adipocyte differentiation.
    Annu Rev Biochem. 1995;64:345-73 PMID: 7574486
  19. Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBP beta is required for hepatocyte proliferation induced by TGF alpha.
    Mol Cell. 1999 Dec;4(6):1087-92 PMID: 10635333
  20. Reciprocity between O-GlcNAc and O-phosphate on the carboxyl terminal domain of RNA polymerase II.
    Biochemistry. 2001 Jul 3;40(26):7845-52 PMID: 11425311
  21. The renaissance of GSK3.
    Nat Rev Mol Cell Biol. 2001 Oct;2(10):769-76 PMID: 11584304
  22. C/EBPalpha arrests cell proliferation through direct inhibition of Cdk2 and Cdk4.
    Mol Cell. 2001 Oct;8(4):817-28 PMID: 11684017
  23. CCAAT/enhancer binding protein-beta is a mediator of keratinocyte survival and skin tumorigenesis involving oncogenic Ras signaling.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):207-12 PMID: 11756662
  24. MEKK1 plays a critical role in activating the transcription factor C/EBP-beta-dependent gene expression in response to IFN-gamma.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):7945-50 PMID: 12048245
  25. Mitotic clonal expansion: a synchronous process required for adipogenesis.
    Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):44-9 PMID: 12502791
  26. CCAAT/enhancer-binding protein beta is required for mitotic clonal expansion during adipogenesis.
    Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):850-5 PMID: 12525691
  27. Dominant-negative C/EBP disrupts mitotic clonal expansion and differentiation of 3T3-L1 preadipocytes.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):43-7 PMID: 14688407
  28. Sequential gene promoter interactions of C/EBPbeta, C/EBPalpha, and PPARgamma during adipogenesis.
    Biochem Biophys Res Commun. 2004 Jun 18;319(1):235-9 PMID: 15158467
  29. Comprehensive proteomic analysis of human pancreatic juice.
    J Proteome Res. 2004 Sep-Oct;3(5):1042-55 PMID: 15473694
  30. Transcriptional activation of the mouse obese (ob) gene by CCAAT/enhancer binding protein alpha.
    Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):873-7 PMID: 8570651
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-07-12
Epub
2005-00-28
Pages
9766-71
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1175002
Subset
IM
Grants
NIDDK NIH HHS · DK 38418 · United States
NIDDK NIH HHS · K01 DK061355 · United States
NIDDK NIH HHS · R01 DK038418 · United States
NIDDK NIH HHS · K01 DK 61355 · United States
PHS HHS · K 61840 · United States
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