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Science 302 (5644): 453-457

Copyright © 2003 by the American Association for the Advancement of Science

Transcriptional Repression of Atherogenic Inflammation: Modulation by PPAR{delta}

Chih-Hao Lee,1 Ajay Chawla,1* Ned Urbiztondo,1 Debbie Liao,1 William A. Boisvert,2 Ronald M. Evans1{dagger}

Abstract: The formation of an atherosclerotic lesion is mediated by lipid-laden macrophages (foam cells), which also establish chronic inflammation associated with lesion progression. The peroxisome proliferator-activated receptor (PPAR) {gamma} promotes lipid uptake and efflux in these atherogenic cells. In contrast, we found that the closely related receptor PPAR{delta} controls the inflammatory status of the macrophage. Deletion of PPAR{delta} from foam cells increased the availability of inflammatory suppressors, which in turn reduced atherosclerotic lesion area by more than 50%. We propose an unconventional ligand-dependent transcriptional pathway in which PPAR{delta} controls an inflammatory switch through its association and disassociation with transcriptional repressors. PPAR{delta} and its ligands may thus serve as therapeutic targets to attenuate inflammation and slow the progression of atherosclerosis.

1 Howard Hughes Medical Institute, Gene Expression Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
2 Vascular Medicine Research, Brigham & Women's Hospital, 65 Landsdowne Street, Room 275, Cambridge, MA 02139, USA.

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* Present address: Division of Endocrinology, Metabolism and Gerontology, Department of Medicine, Stanford University, Stanford, CA 94305, USA.

{dagger} To whom correspondence should be addressed. E-mail: evans{at}salk.edu


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PPAR{delta} regulates glucose metabolism and insulin sensitivity.
C.-H. Lee, P. Olson, A. Hevener, I. Mehl, L.-W. Chong, J. M. Olefsky, F. J. Gonzalez, J. Ham, H. Kang, J. M. Peters, et al. (2006)
PNAS 103, 3444-3449
   Abstract »    Full Text »    PDF »
Emerging Therapies Targeting High-Density Lipoprotein Metabolism and Reverse Cholesterol Transport.
D. Duffy and D. J. Rader (2006)
Circulation 113, 1140-1150
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Peroxisome proliferator-activated receptor {delta} promotes very low-density lipoprotein-derived fatty acid catabolism in the macrophage.
C.-H. Lee, K. Kang, I. R. Mehl, R. Nofsinger, W. A. Alaynick, L.-W. Chong, J. M. Rosenfeld, and R. M. Evans (2006)
PNAS 103, 2434-2439
   Abstract »    Full Text »    PDF »
Protection against Fatty Liver but Normal Adipogenesis in Mice Lacking Adipose Differentiation-Related Protein.
B. H.-J. Chang, L. Li, A. Paul, S. Taniguchi, V. Nannegari, W. C. Heird, and L. Chan (2006)
Mol. Cell. Biol. 26, 1063-1076
   Abstract »    Full Text »    PDF »
Obesity, Peroxisome Proliferator-Activated Receptor, and Atherosclerosis in Type 2 Diabetes.
F. Blaschke, Y. Takata, E. Caglayan, R. E. Law, and W. A. Hsueh (2006)
Arterioscler Thromb Vasc Biol 26, 28-40
   Abstract »    Full Text »    PDF »
14,15-Dihydroxyeicosatrienoic acid activates peroxisome proliferator-activated receptor-{alpha}.
X. Fang, S. Hu, B. Xu, G. D. Snyder, S. Harmon, J. Yao, Y. Liu, B. Sangras, J. R. Falck, N. L. Weintraub, et al. (2006)
Am J Physiol Heart Circ Physiol 290, H55-H63
   Abstract »    Full Text »    PDF »
IGF-1 induces rat glomerular mesangial cells to accumulate triglyceride.
A. K. Berfield, A. Chait, J. F. Oram, R. A. Zager, A. C. Johnson, and C. K. Abrass (2006)
Am J Physiol Renal Physiol 290, F138-F147
   Abstract »    Full Text »    PDF »
Swine Models of Type 2 Diabetes Mellitus: Insulin Resistance, Glucose Tolerance, and Cardiovascular Complications.
D. A. Bellinger, E. P. Merricks, and T. C. Nichols (2006)
ILAR J 47, 243-258
   Abstract »    Full Text »    PDF »
Proteomic and Transcriptomic Analyses of Macrophages with an Increased Resistance to Oxidized Low Density Lipoprotein (oxLDL)-induced Cytotoxicity Generated by Chronic Exposure to oxLDL.
J. P. Conway and M. Kinter (2005)
Mol. Cell. Proteomics 4, 1522-1540
   Abstract »    Full Text »    PDF »
Therapeutic Roles of Peroxisome Proliferator-Activated Receptor Agonists.
B. Staels and J.-C. Fruchart (2005)
Diabetes 54, 2460-2470
   Abstract »    Full Text »    PDF »
Prostacyclin signaling in the kidney: implications for health and disease.
R. Nasrallah and R. L. Hebert (2005)
Am J Physiol Renal Physiol 289, F235-F246
   Abstract »    Full Text »    PDF »
Peroxisome Proliferator-Activated Receptor {beta}/{delta} Exerts a Strong Protection from Ischemic Acute Renal Failure.
E. Letavernier, J. Perez, E. Joye, A. Bellocq, B. Fouqueray, J.-P. Haymann, D. Heudes, W. Wahli, B. Desvergne, and L. Baud (2005)
J. Am. Soc. Nephrol. 16, 2395-2402
   Abstract »    Full Text »    PDF »
Antiinflammatory Effects of Tetradecylthioacetic Acid Involve Both Peroxisome Proliferator-Activated Receptor {alpha}-Dependent and -Independent Pathways.
E. Dyroy, A. Yndestad, T. Ueland, B. Halvorsen, J. K. Damas, P. Aukrust, and R. K. Berge (2005)
Arterioscler Thromb Vasc Biol 25, 1364-1369
   Abstract »    Full Text »    PDF »
Modulation of Peroxisome Proliferator-Activated Receptor {delta} Activity Affects Neural Cell Adhesion Molecule and Polysialyltransferase ST8SiaIV Induction by Teratogenic Valproic Acid Analogs in F9 Cell Differentiation.
A. Lampen, P. A. Grimaldi, and H. Nau (2005)
Mol. Pharmacol. 68, 193-203
   Abstract »    Full Text »    PDF »
Peroxisome Proliferator-Activated Receptor {delta} and {gamma} Agonists Differentially Alter Tumor Differentiation and Progression during Mammary Carcinogenesis.
Y. Yin, R. G. Russell, L. E. Dettin, R. Bai, Z.-L. Wei, A. P. Kozikowski, L. Kopleovich, and R. I. Glazer (2005)
Cancer Res. 65, 3950-3957
   Abstract »    Full Text »    PDF »
Effects of peroxisome proliferator-activated receptor {alpha}/{delta} agonists on HDL-cholesterol in vervet monkeys.
J. M. Wallace, M. Schwarz, P. Coward, J. Houze, J. K. Sawyer, K. L. Kelley, A. Chai, and L. L. Rudel (2005)
J. Lipid Res. 46, 1009-1016
   Abstract »    Full Text »    PDF »
Dehydroepiandrosterone Can Inhibit the Proliferation of Myeloma Cells and the Interleukin-6 Production of Bone Marrow Mononuclear Cells from Patients with Myeloma.
S. Liu, H. Ishikawa, F.-J. Li, Z. Ma, K.-i. Otsuyama, H. Asaoku, S. Abroun, X. Zheng, N. Tsuyama, M. Obata, et al. (2005)
Cancer Res. 65, 2269-2276
   Abstract »    Full Text »    PDF »
Peroxisome Proliferator-activated Receptor-{beta}/{delta} Inhibits Epidermal Cell Proliferation by Down-regulation of Kinase Activity.
D. J. Kim, I. A. Murray, A. M. Burns, F. J. Gonzalez, G. H. Perdew, and J. M. Peters (2005)
J. Biol. Chem. 280, 9519-9527
   Abstract »    Full Text »    PDF »
Peroxisome Proliferation-Activated Receptor (PPAR){gamma} Is Not Necessary for Synthetic PPAR{gamma} Agonist Inhibition of Inducible Nitric-Oxide Synthase and Nitric Oxide.
M. B. Crosby, J. L. Svenson, J. Zhang, C. J. Nicol, F. J. Gonzalez, and G. S. Gilkeson (2005)
J. Pharmacol. Exp. Ther. 312, 69-76
   Abstract »    Full Text »    PDF »
PPAR- and LXR-dependent pathways controlling lipid metabolism and the development of atherosclerosis.
A. C. Li and C. K. Glass (2004)
J. Lipid Res. 45, 2161-2173
   Abstract »    Full Text »    PDF »
Peroxisome Proliferator-Activated Receptor Family and Its Relationship to Renal Complications of the Metabolic Syndrome.
Y. Guan (2004)
J. Am. Soc. Nephrol. 15, 2801-2815
   Abstract »    Full Text »    PDF »
Essential role of Smad3 in the inhibition of inflammation-induced PPAR{beta}/{delta} expression.
N. S. Tan, L. Michalik, N. Di-Poi, C. Y. Ng, N. Mermod, A. B. Roberts, B. Desvergne, and W. Wahli (2004)
EMBO J. 23, 4211-4221
   Abstract »    Full Text »    PDF »
Modulation of Uncoupling Protein 1 and Peroxisome Proliferator-Activated Receptor {gamma} Expression in Adipose Tissue in Obese Insulin-Resistant Dogs.
V. Leray, C. Gayet, L. Martin, H. Dumon, B. Siliart, and P. Nguyen (2004)
J. Nutr. 134, 2154S-2157S
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