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J. Biol. Chem., Vol. 280, Issue 20, 20094-20101, May 20, 2005

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Intestinal Glucose-dependent Expression of Glucose-6-phosphatase

INVOLVEMENT OF THE ARYL RECEPTOR NUCLEAR TRANSLOCATOR TRANSCRIPTION FACTOR^*

Véronique Carrière, Maude Le Gall, Florence Gouyon-Saumande, Dieter Schmoll¶, Edith Brot-Laroche, Valérie Chauffeton, Jean Chambaz, and Monique Rousset

From the INSERM UMR 505, Université Pierre et Marie Curie, Paris F-75006, France and ^¶Sanofi-Aventis Pharma, DG Metabolic Diseases, Frankfurt D-65926, Germany

Glucose-6-phosphatase (G6Pase) catalyzes the release of glucose from glucose 6-phosphate. This enzyme was mainly studied in the liver, but while detected in the small intestine little is known about the regulation of its intestinal expression. This study describes the mechanisms of the glucose-dependent regulation of G6Pase expression in intestinal cells. Results obtained in vivo and in Caco-2/TC7 enterocytes showed that glucose increases the G6Pase mRNA level. In Caco-2/TC7 cells, glucose stabilized G6Pase mRNA and activated the transcription of the gene, meaning that glucose-dependent G6Pase expression involved both transcriptional and post-transcriptional mechanisms. Reporter-gene studies showed that, although the –299/+57 region of the human G6Pase promoter was sufficient to trigger the glucose response in the hepatoma cell line HepG2, the –1157/–1133 fragment was required for maximal activation of glucose-6-phosphatase gene transcription in Caco-2/TC7 cells. This fragment binds the aryl receptor nuclear translocator (ARNT), cAMP-responsive element-binding protein, and upstream stimulatory factor transcription factors. The DNA binding activity of these transcription factors was increased in nuclear extracts of differentiated cells from the intestinal villus of mice fed sugar-rich diets as compared with mice fed a no-sugar diet. A direct implication of ARNT in the activation of G6Pase gene transcription by glucose has been observed in Caco-2/TC7 cells using RNA interference experiments. These results support a physiological role for G6Pase in the control of nutrient absorption in the small intestine.

Received for publication, February 25, 2005

^* This work was supported in part by ATC Nutrition INSERM Grant ASE02129DSA. 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.

To whom correspondence should be addressed: UMR505, Centre de Recherches Biomédicales des Cordeliers, 15 rue de l'Ecole de Médecine, 75006 Paris, France. Tel.: 33-1-42-34-69-34; Fax: 33-1-43-25-16-15; E-mail: veronique.carriere-u505{at}bhdc.jussieu.fr.

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