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
-
Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes.
J Biol Chem. 1980 May 25;255(10):4745-50
PMID: 7372608
-
A new technique for the assay of infectivity of human adenovirus 5 DNA.
Virology. 1973 Apr;52(2):456-67
PMID: 4705382
-
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
-
The organization, promoter analysis, and expression of the human PPARgamma gene.
J Biol Chem. 1997 Jul 25;272(30):18779-89
PMID: 9228052
-
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
-
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
-
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
-
CCAAT-enhancer binding protein: a component of a differentiation switch.
Science. 1991 Jan 18;251(4991):288-92
PMID: 1987644
-
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
-
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
-
Calcium-regulated phosphorylation within the leucine zipper of C/EBP beta.
Science. 1992 Apr 17;256(5055):370-3
PMID: 1314426
-
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
-
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
-
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
-
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
-
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
-
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
-
Transcriptional regulation of gene expression during adipocyte differentiation.
Annu Rev Biochem. 1995;64:345-73
PMID: 7574486
-
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
-
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
-
The renaissance of GSK3.
Nat Rev Mol Cell Biol. 2001 Oct;2(10):769-76
PMID: 11584304
-
C/EBPalpha arrests cell proliferation through direct inhibition of Cdk2 and Cdk4.
Mol Cell. 2001 Oct;8(4):817-28
PMID: 11684017
-
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
-
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
-
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
-
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
-
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
-
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
-
Comprehensive proteomic analysis of human pancreatic juice.
J Proteome Res. 2004 Sep-Oct;3(5):1042-55
PMID: 15473694
-
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