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A more recent version of this article appeared on April 29, 2005
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M500403200v1
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Papers In Press, published online ahead of print February 14, 2005
J. Biol. Chem, 10.1074/jbc.M500403200
Submitted on January 12, 2005
Revised on February 14, 2005
Accepted on February 14, 2005

Cyclin D1 inhibits PPARgamma -mediated adipogenesis through HDAC recruitment

Maofu Fu, Mahadev Rao, Toula Bouras, Chenguang Wang, Kongming Wu, Xueping Zhang, Zhiping Li, Tiso-Pang Yao, and Richard G. Pestell

Department of Oncology, Georgetown University, Washington,, DC 20057-1468

Corresponding Author: pestell{at}georgetown.edu

The cyclin D1 gene encodes the labile serum-inducible regulatory subunit of a holoenzyme that phosphorylates and inactivates the retinoblastoma protein. Overexpression of cyclin D1 promotes cellular proliferation and normal physiological levels of cyclin D1 function to inhibit adipocyte differentiation in vivo. We have previously shown that cyclin D1 inhibits PPARgamma-dependent activity through a Cdk- and Rb-binding independent mechanism. In this study, we determined the molecular mechanism by which cyclin D1 regulated PPARgamma function. Herein, MEF (murine embryonic fibroblast)differentiation by PPARgamma ligand was associated with a reduction in HDAC1 activity. Cyclin D1-/- MEFs showed increased propensity to undergo differentiation into adipocytes. Genetic deletion of cyclin D1 reduced HDAC1 activity. Reconstitution of cyclin D1 into the cyclin D1-/- MEFs increased HDAC1 activity and blocked PPARgamma-mediated adipogenesis. PPARgamma activity was enhanced in cyclin D1-/- cells. Reintroduction of cyclin D1 inhibited basal and ligand-induced PPARgamma activity and enhanced HDAC repression of PPARgamma activity. Cyclin D1 bound HDAC in vivo and preferentially physically associated with HDAC1, HDAC2, HDAC3 and HDAC5. Chromatin immunoprecipitation assay demonstrated that cyclin D1 enhanced recruitment of HDAC1 and 3 and histone methyltransferase SUV39H1 to the PPARE of the LPL promoter and decreased acetylation of total histone H3 and histone H3 lysine 9. Collectively, these studies suggest an important role of cyclin D1 in regulation of PPARgamma-mediated adipocyte differentiation through recruitment of HDACs to regulate PPARE local chromatin structure and PPARgamma function.


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