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Originally published In Press as doi:10.1074/jbc.M205087200 on July 9, 2002

J. Biol. Chem., Vol. 277, Issue 41, 37991-38000, October 11, 2002
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The Coactivator PGC-1 Is Involved in the Regulation of the Liver Carnitine Palmitoyltransferase I Gene Expression by cAMP in Combination with HNF4alpha and cAMP-response Element-binding Protein (CREB)*

Jean-François LouetDagger , Graham Hayhurst§, Frank J. Gonzalez||, Jean GirardDagger , and Jean-François DecauxDagger **

From the Dagger  Institut Cochin, Département d'Endocrinologie, 24 rue du Faubourg Saint Jacques, 75014 Paris, France, the § Unité de Génétique de la Différenciation, Département de Biologie du Développement, Institut Pasteur, 25/28 rue du Dr. Roux, 75015 Paris, France, and the || Laboratory of Metabolism, Division of Basic Sciences, NCI, National Institutes of Health, Bethesda, Maryland 20892

Liver carnitine palmitoyltransferase I catalyzes the transfer of long-chain fatty acids into mitochondria. L-CPT I is considered the rate-controlling enzyme in fatty acid oxidation. Expression of the L-CPT I gene is induced by starvation in response to glucagon secretion from the pancreas, an effect mediated by cAMP. Here, the molecular mechanisms underlying the induction of L-CPT I gene expression by cAMP were characterized. We demonstrate that the cAMP response unit of the L-CPT I gene is composed of a cAMP-response element motif and a DR1 sequence located 3 kb upstream of the transcription start site. Our data strongly suggest that the coactivator PGC-1 is involved in the regulation of this gene expression by cAMP in combination with HNF4alpha and cAMP-response element-binding protein (CREB). Indeed, (i) cotransfection of CREB or HNF4alpha dominant negative mutants completely abolishes the effect of cAMP on the L-CPT I promoter, and (ii) the cAMP-responsive unit binds HNF4alpha and CREB through the DR1 and the cAMP-response element sequences, respectively. Moreover, cotransfection of PGC-1 strongly activates the L-CPT I promoter through HNF4alpha bound at the DR1 element. Finally, we show that the transcriptional induction of the PGC-1 gene by glucagon through cAMP in hepatocytes precedes that of L-CPT-1. In addition to the key role that PGC-1 plays in glucose homeostasis, it may also be critical for lipid homeostasis. Taken together these observations suggest that PGC-1 acts to coordinate the process of metabolic adaptation in the liver.

* This work was supported by the Fondation pour la recherche médicale and the Fondation Bettencourt-Schueller.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.

This paper is dedicated to the memory of J. D. McGarry who passed away on January 27, 2002.

Supported through a European Community Marie Curie Fellowship.

** To whom correspondence should be addressed. Tel.: 33-1-53-73-27-06; Fax: 33-1-53-73-27-03; E-mail: decaux@cochin.inserm.fr.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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