Inhibition of Cellular Proliferation through I{kappa}B Kinase-Independent and Peroxisome Proliferator-Activated Receptor {gamma}-Dependent Repression of Cyclin D1

doi:10.1128/MCB.21.9.3057-3070.2001

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Molecular and Cellular Biology, May 2001, p. 3057-3070, Vol. 21, No. 9
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.9.3057-3070.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Inhibition of Cellular Proliferation through I $kappa$ B Kinase-Independent and Peroxisome Proliferator-Activated Receptor $gamma$ -Dependent Repression of Cyclin D1

Chenguang Wang,¹ Maofu Fu,¹ Mark D'Amico,¹ Chris Albanese,¹ Jian-Nian Zhou,¹ Michael Brownlee,¹ Michael P. Lisanti,² V. Krishna K. Chatterjee,³ Mitchell A. Lazar,⁴ and Richard G. Pestell¹^,^*

Departments of Developmental and Molecular Biology and Medicine, The Albert Einstein Cancer Center,¹ and Department of Pharmacology, Albert Einstein College of Medicine,² Bronx, New York 10461; Department of Medicine, University of Cambridge, Addenbrooke's Hospital, Cambridge CB2 2QQ, United Kingdom³; and Division of Endocrinology, Diabetes, and Metabolism, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104⁴

Received 6 September 2000/Returned for modification 9 October 2000/Accepted 13 February 2001

The nuclear receptor peroxisome proliferator-activated receptor $gamma$ (PPAR $gamma$ ) is a ligand-regulated nuclear receptor superfamilymember. Liganded PPAR $gamma$ exerts diverse biological effects, promotingadipocyte differentiation, inhibiting tumor cellular proliferation,and regulating monocyte/macrophage and anti-inflammatory activitiesin vitro. In vivo studies with PPAR $gamma$ ligands showed enhancementof tumor growth, raising the possibility that reduced immune functionand tumor surveillance may outweigh the direct inhibitory effectsof PPAR $gamma$ ligands on cellular proliferation. Recent findings thatPPAR $gamma$ ligands convey PPAR $gamma$ -independent activities through I $kappa$ Bkinase (IKK) raises important questions about the specific mechanismsthrough which PPAR $gamma$ ligands inhibit cellular proliferation. Weinvestigated the mechanisms regulating the antiproliferative effectof PPAR $gamma$ . Herein PPAR $gamma$ , liganded by either natural (15d-PGJ₂ andPGD₂) or synthetic ligands (BRL49653 and troglitazone), selectivelyinhibited expression of the cyclin D1 gene. The inhibition ofS-phase entry and activity of the cyclin D1-dependent serine-threoninekinase (Cdk) by 15d-PGJ₂ was not observed in PPAR $gamma$ -deficient cells.Cyclin D1 overexpression reversed the S-phase inhibition by 15d-PGJ₂.Cyclin D1 repression was independent of IKK, as prostaglandins(PGs) which bound PPAR $gamma$ but lacked the IKK interactive cyclopentonering carbonyl group repressed cyclin D1. Cyclin D1 repressionby PPAR $gamma$ involved competition for limiting abundance of p300,directed through a c-Fos binding site of the cyclin D1 promoter.15d-PGJ₂ enhanced recruitment of p300 to PPAR $gamma$ but reduced bindingto c-Fos. The identification of distinct pathways through whicheicosanoids regulate anti-inflammatory and antiproliferative effectsmay improve the utility of COX2inhibitors.

^* Corresponding author. Mailing address: The Albert Einstein Cancer Center, Department of Developmental and Molecular Biology,Albert Einstein College of Medicine, Chanin 302, 1300 Morris ParkAve., Bronx, NY 10461. Phone: (718) 430-8662. Fax: (718) 430-8674.E-mail: pestell{at}aecom.yu.edu.

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Inhibition of Cellular Proliferation through IB Kinase-Independent and Peroxisome Proliferator-Activated Receptor -Dependent Repression of Cyclin D1

Inhibition of Cellular Proliferation through I $kappa$ B Kinase-Independent and Peroxisome Proliferator-Activated Receptor $gamma$ -Dependent Repression of Cyclin D1