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Mediate in Vivo Regulation of Uncoupling Protein (UCP-1, UCP-2, UCP-3) Gene Expression
Departments of Molecular Endocrinology (L.J.K., G.M.T., T.W.D., J.V., M.S.W., D.E.M.), Molecular Pharmacology and Biochemistry (P.P.V., M.R.C., M.A.C.), and Cellular and Molecular Pharmacology (R.M., M.J.F.), Merck Research Laboratories, Rahway, New Jersey 07065; and Department of Safety Assessment (M.W.C.), Merck Research Laboratories, West Point, Pennsylvania 19486
Address all correspondence and requests for reprints to: Dr. Linda Kelly, Merck Research Laboratories, 80W-207 P.O. Box 2000, Rahway, New Jersey 07065. E-mail: kelly_linda{at}merck.com
A role for peroxisome proliferator-activated receptors, PPAR
and
PPAR
, as regulators of energy homeostasis and lipid metabolism, has
been suggested. Recently, three distinct uncoupling protein isoforms,
UCP-1, UCP-2, and UCP-3, have also been identified and implicated as
mediators of thermogenesis. Here, we examined whether in
vivo PPAR or PPAR activation regulates the expression of
all three UCP isoforms. Rats or lean and db/db mice were
treated with PPAR [thiazolidinedione (TZD)] or PPAR (WY-14643)
agonists, followed by measurement of messenger RNAs (mRNAs) for
UCP-1, UCP-2, and UCP-3 in selected tissues where they are expressed.
TZD treatment (AD 5075 at 5 mg/kg·day) of rats (14 days) increased
brown adipose tissue (BAT) depot size and induced the expression of
each UCP mRNA (3x control levels for UCP-1 and UCP-2, 2.5x control
for UCP-3). In contrast, UCP-2 and UCP-3 mRNA levels were not affected
in white adipose tissue or skeletal muscle. Chronic (30 days) low-dose
(0.3 mg/kg·day) TZD treatment induced UCP-1 mRNA and protein in BAT
(2.5x control). In contrast, chronic TZD treatment (30 mg/kg·day)
suppressed UCP-1 mRNA (>80%) and protein (50%) expression in BAT.
This was associated with further induction of UCP-2 expression
(>10-fold) and an increase in the size of lipid vacuoles, a decrease
in the number of lipid vacuoles in each adipocyte, and an increase in
the size of the adipocytes. TZD treatment of db/db mice
(BRL 49653 at 10 mg/kg·day for 10 days) also induced
UCP-1 and UCP-3 (but not UCP-2) expression in BAT. PPAR is present
in BAT, as well as liver. Treatment of rats or db/db
mice with WY-14643 did not affect expression of UCP-1, -2, or -3 in
BAT. Hepatic UCP-2 mRNA was increased (4x control level) in
db/db and lean mice, although this effect was not
observed in rats. Thus, in vivo PPAR activation can
induce expression of UCP-1, -2, and -3 in BAT; whereas chronic-intense
PPAR activation may cause BAT to assume white adipose tissue-like
phenotype with increased UCP-2 levels. PPAR activation in mice is
sufficient to induce liver UCP-2 expression.
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S. Viengchareun, P. Penfornis, M.-C. Zennaro, and M. Lombes Mineralocorticoid and glucocorticoid receptors inhibit UCP expression and function in brown adipocytes Am J Physiol Endocrinol Metab, April 1, 2001; 280(4): E640 - E649. [Abstract] [Full Text] [PDF]
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T. Albrektsen and J. Fleckner The Transcription Factor Fos-Related Antigen 1 Is Induced by Thiazolidinediones During Differentiation of 3T3-L1 Cells Mol. Pharmacol., March 1, 2001; 59(3): 567 - 575. [Abstract] [Full Text]
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R. A. Memon, L. H. Tecott, K. Nonogaki, A. Beigneux, A. H. Moser, C. Grunfeld, and K. R. Feingold Up-Regulation of Peroxisome Proliferator-Activated Receptors (PPAR-{alpha}) and PPAR-{gamma} Messenger Ribonucleic Acid Expression in the Liver in Murine Obesity: Troglitazone Induces Expression of PPAR-{gamma}-Responsive Adipose Tissue-Specific Genes in the Liver of Obese Diabetic Mice Endocrinology, November 1, 2000; 141(11): 4021 - 4031. [Abstract] [Full Text] [PDF]
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X. X. Yu, J. L. Barger, B. B. Boyer, M. D. Brand, G. Pan, and S. H. Adams Impact of endotoxin on UCP homolog mRNA abundance, thermoregulation, and mitochondrial proton leak kinetics Am J Physiol Endocrinol Metab, August 1, 2000; 279(2): E433 - E446. [Abstract] [Full Text] [PDF]
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 K. A. J. M. VAN DER LEE, P. H. M. WILLEMSEN, G. J. VAN DER VUSSE, and M. VAN BILSEN Effects of fatty acids on uncoupling protein-2 expression in the rat heart FASEB J, March 1, 2000; 14(3): 495 - 502. [Abstract] [Full Text]
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 B. Desvergne and W. Wahli Peroxisome Proliferator-Activated Receptors: Nuclear Control of Metabolism Endocr. Rev., October 1, 1999; 20(5): 649 - 688. [Abstract] [Full Text]
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A. Matthias, A. Jacobsson, B. Cannon, and J. Nedergaard The Bioenergetics of Brown Fat Mitochondria from UCP1-ablated Mice. UCP1 IS NOT INVOLVED IN FATTY ACID-INDUCED DE-ENERGIZATION ("UNCOUPLING") J. Biol. Chem., October 1, 1999; 274(40): 28150 - 28160. [Abstract] [Full Text] [PDF]
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L. Poretsky, N. A. Cataldo, Z. Rosenwaks, and L. C. Giudice The Insulin-Related Ovarian Regulatory System in Health and Disease Endocr. Rev., August 1, 1999; 20(4): 535 - 582. [Abstract] [Full Text] [PDF]
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M. J. Barbera, A. Schluter, N. Pedraza, R. Iglesias, F. Villarroya, and M. Giralt Peroxisome Proliferator-activated Receptor alpha Activates Transcription of the Brown Fat Uncoupling Protein-1 Gene. A LINK BETWEEN REGULATION OF THE THERMOGENIC AND LIPID OXIDATION PATHWAYS IN THE BROWN FAT CELL J. Biol. Chem., January 5, 2001; 276(2): 1486 - 1493. [Abstract] [Full Text] [PDF]
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A. V. Medvedev, S. K. Snedden, S. Raimbault, D. Ricquier, and S. Collins Transcriptional Regulation of the Mouse Uncoupling Protein-2 Gene. DOUBLE E-BOX MOTIF IS REQUIRED FOR PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR-gamma -DEPENDENT ACTIVATION J. Biol. Chem., March 30, 2001; 276(14): 10817 - 10823. [Abstract] [Full Text] [PDF]
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T. Yamauchi, J. Kamon, H. Waki, K. Murakami, K. Motojima, K. Komeda, T. Ide, N. Kubota, Y. Terauchi, K. Tobe, et al. The Mechanisms by Which Both Heterozygous Peroxisome Proliferator-activated Receptor gamma (PPARgamma ) Deficiency and PPARgamma Agonist Improve Insulin Resistance J. Biol. Chem., October 26, 2001; 276(44): 41245 - 41254. [Abstract] [Full Text] [PDF]
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N. M. Morton, M. C. Holmes, C. Fievet, B. Staels, A. Tailleux, J. J. Mullins, and J. R. Seckl Improved Lipid and Lipoprotein Profile, Hepatic Insulin Sensitivity, and Glucose Tolerance in 11beta -Hydroxysteroid Dehydrogenase Type 1 Null Mice J. Biol. Chem., October 26, 2001; 276(44): 41293 - 41300. [Abstract] [Full Text] [PDF]
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Y. Nagai, Y. Nishio, T. Nakamura, H. Maegawa, R. Kikkawa, and A. Kashiwagi Amelioration of high fructose-induced metabolic derangements by activation of PPARalpha Am J Physiol Endocrinol Metab, May 1, 2002; 282(5): E1180 - E1190. [Abstract] [Full Text] [PDF]
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