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J. Biol. Chem., Vol. 277, Issue 29, 26089-26097, July 19, 2002
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From the Ablation of peroxisome proliferator
activated receptor (PPAR)
Fatty Acid Homeostasis and Induction of Lipid Regulatory
Genes in Skeletal Muscles of Peroxisome Proliferator-activated
Receptor (PPAR)
Knock-out Mice
EVIDENCE FOR COMPENSATORY REGULATION BY PPAR
*
§,,
,,
Departments of Medicine and Cell Biology,
Duke University Medical Center, Durham, North Carolina 27710, the
¶ Department of Biochemistry and the Human Performance Laboratory,
East Carolina University, Greenville, North Carolina 27858, the
Departments of Metabolic Diseases and Nuclear Receptor Biology,
GlaxoSmithKline, Research Triangle Park, North Carolina 27709, and the
** Chemical Industry Institute of Toxicology
Centers for Health Research,
Research Triangle Park, North Carolina 27709
, a lipid-activated transcription factor
that regulates expression of 
-oxidative genes, results in profound
metabolic abnormalities in liver and heart. In the present study we
used PPAR knockout (KO) mice to determine whether this transcription
factor is essential for regulating fuel metabolism in skeletal muscle.
When animals were challenged with exhaustive exercise or starvation, KO
mice exhibited lower serum levels of glucose, lactate, and ketones and
higher nonesterified fatty acids than wild type (WT) littermates. During exercise, KO mice exhausted earlier than WT and exhibited greater rates of glycogen depletion in liver but not skeletal muscle.
Fatty acid oxidative capacity was similar between muscles of WT and KO
when animals were fed and only 28% lower in KO muscles when animals
were starved. Exercise-induced regulation and starvation-induced regulation of pyruvate-dehydrogenase kinase 4 and uncoupling
protein 3, two classical and robustly responsive PPAR target genes,
were similar between WT and KO in skeletal muscle but markedly
different between genotypes in heart. Real time quantitative PCR
analyses showed that unlike in liver and heart, in mouse skeletal
muscle PPAR is severalfold more abundant than either PPAR or
PPAR
. In both human and rodent myocytes, the highly selective
PPAR agonist GW742 increased fatty acid oxidation about 2-fold and induced expression of several lipid regulatory genes, including pyruvate-dehydrogenase kinase 4 and uncoupling protein 3, responses that were similar to those elicited by the PPAR agonist GW647. These
results show redundancy in the functions of PPARs and as
transcriptional regulators of fatty acid homeostasis and suggest that
in skeletal muscle high levels of the -subtype can compensate for
deficiency of PPAR.
*
This work was supported by National Institutes of Health
Grants 46121-06 (to G. L. D.), F32DK 10017-01 (to D. M. M.) and HL57354 (to W. E. K.) and a grant from the
North Carolina Institute of Nutrition (to D. M. M. and
J. A. H.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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A. P. Russell, J. Feilchenfeldt, S. Schreiber, M. Praz, A. Crettenand, C. Gobelet, C. A. Meier, D. R. Bell, A. Kralli, J.-P. Giacobino, et al. Endurance Training in Humans Leads to Fiber Type-Specific Increases in Levels of Peroxisome Proliferator-Activated Receptor-{gamma} Coactivator-1 and Peroxisome Proliferator-Activated Receptor-{alpha} in Skeletal Muscle Diabetes, December 1, 2003; 52(12): 2874 - 2881. [Abstract] [Full Text] [PDF]
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H. Koutnikova, T.-A. Cock, M. Watanabe, S. M. Houten, M.-F. Champy, A. Dierich, and J. Auwerx Compensation by the muscle limits the metabolic consequences of lipodystrophy in PPAR{gamma} hypomorphic mice PNAS, November 25, 2003; 100(24): 14457 - 14462. [Abstract] [Full Text] [PDF]
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 K. E. Schmid and L. A. Woollett Differential effects of polyunsaturated fatty acids on sterol synthesis rates in adult and fetal tissues of the hamster: consequence of altered sterol balance Am J Physiol Gastrointest Liver Physiol, November 1, 2003; 285(5): G796 - G803. [Abstract] [Full Text] [PDF]
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H. J. Grav, K. J. Tronstad, O. A. Gudbrandsen, K. Berge, K. E. Fladmark, T. C. Martinsen, H. Waldum, H. Wergedahl, and R. K. Berge Changed Energy State and Increased Mitochondrial {beta}-Oxidation Rate in Liver of Rats Associated with Lowered Proton Electrochemical Potential and Stimulated Uncoupling Protein 2 (UCP-2) Expression: EVIDENCE FOR PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR-{alpha} INDEPENDENT INDUCTION OF UCP-2 EXPRESSION J. Biol. Chem., August 15, 2003; 278(33): 30525 - 30533. [Abstract] [Full Text] [PDF]
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C.-H. Lee, P. Olson, and R. M. Evans Minireview: Lipid Metabolism, Metabolic Diseases, and Peroxisome Proliferator-Activated Receptors Endocrinology, June 1, 2003; 144(6): 2201 - 2207. [Abstract] [Full Text] [PDF]
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M. C. Sugden and M. J. Holness Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs Am J Physiol Endocrinol Metab, May 1, 2003; 284(5): E855 - E862. [Abstract] [Full Text] [PDF]
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 K. Bae and D. R. Weaver Light-Induced Phase Shifts in Mice Lacking mPER1 or mPER2 J Biol Rhythms, April 1, 2003; 18(2): 123 - 133. [Abstract] [PDF]
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A. J. Gilde, K. A.J.M. van der Lee, P. H.M. Willemsen, G. Chinetti, F. R. van der Leij, G. J. van der Vusse, B. Staels, and M. van Bilsen Peroxisome Proliferator-Activated Receptor (PPAR) {alpha} and PPAR{beta}/{delta}, but not PPAR{gamma}, Modulate the Expression of Genes Involved in Cardiac Lipid Metabolism Circ. Res., March 21, 2003; 92(5): 518 - 524. [Abstract] [Full Text] [PDF]
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E. A. Turvey, G. J. F. Heigenhauser, M. Parolin, and S. J. Peters Elevated n-3 fatty acids in a high-fat diet attenuate the increase in PDH kinase activity but not PDH activity in human skeletal muscle J Appl Physiol, January 1, 2005; 98(1): 350 - 355. [Abstract] [Full Text] [PDF]
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