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J. Biol. Chem., Vol. 279, Issue 50, 52052-52058, December 10, 2004
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Estrogen-related Receptor 
(ERR) Is a Transcriptional Regulator of Apolipoprotein A-IV and Controls Lipid Handling in the Intestine*
||**
From the
Molecular Oncology Group, McGill University Health Center, Montréal, Québec H3A 1A1, Canada, the ¶Centre de Recherche, Hôpital Sainte-Justine, Département de Nutrition, Université de Montréal, Montréal, Québec H3C 1C5, Canada, and the ||Departments of Biochemistry, Medicine, and Oncology, McGill University, Montréal, Québec H3A 1A1, Canada
The estrogen-related receptor 
(ERR) is an orphan member of the superfamily of nuclear receptors involved in the control of energy metabolism. In particular, ERR induces a high energy expenditure in the presence of the coactivator PGC-1. However, ERR knockout mice have reduced fat mass and are resistant to diet-induced obesity. ERR is expressed in epithelial cells of the small intestine, and because the intestine is the first step in the energy chain, we investigated whether ERR plays a function in dietary energy handling. Gene expression profiling in the intestine identified a subset of genes involved in oxidative phosphorylation that were down-regulated in the absence of ERR. In support of the physiological role of ERR in this pathway, isolated enterocytes from ERR knockout mice display lower capacity for 
-oxidation. Microarray results also show altered expression of genes involved in dietary lipid digestion and absorption, such as pancreatic lipase-related protein 2 (PLRP2), fatty acid-binding protein 1 and 2 (L-FABP and I-FABP), and apolipoprotein A-IV (apoA-IV). In agreement, we found that ERR–/– pups exhibit significant lipid malabsorption. We further show that the apoA-IV promoter is a direct target of ERR and that its presence is required to maintain basal level but not feeding-induced regulation of the apoA-IV gene in mice. ERR, in cooperation with PGC-1, activates the apoA-IV promoter via interaction with the apoC-III enhancer in both human and mouse. Our results demonstrate that apoA-IV is a direct ERR target gene and suggest a function for ERR in intestinal fat transport, a crucial step in energy balance.
Received for publication, September 9, 2004 , and in revised form, September 30, 2004.
* This work was supported by the Canadian Institutes for Health Research (CIHR). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Recipient of a CIHR fellowship.
** Recipient of a CIHR senior scientist career award. To whom correspondence should be addressed: Molecular Oncology Group, McGill University Health Centre, Room H5–21, 687 Pine Ave. W., Montréal, Québec H3A 1A1, Canada. Tel.: 514-843-1406; Fax: 514-843-1478; E-mail: vincent.giguere{at}mcgill.ca.
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