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Articles, Behavioral/Systems/Cognitive

Food Intake Adaptation to Dietary Fat Involves PSA-Dependent Rewiring of the Arcuate Melanocortin System in Mice

Alexandre Benani, Cécile Hryhorczuk, Alexandra Gouazé, Xavier Fioramonti, Xavier Brenachot, Christophe Guissard, Alice Krezymon, Thibaut Duparc, André Colom, Emmanuelle Nédélec, Caroline Rigault, Aleth Lemoine, Jean Gascuel, Rita Gerardy-Schahn, Philippe Valet, Claude Knauf, Anne Lorsignol and Luc Pénicaud
Journal of Neuroscience 29 August 2012, 32 (35) 11970-11979; https://doi.org/10.1523/JNEUROSCI.0624-12.2012
Alexandre Benani
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Cécile Hryhorczuk
2STROMAlab; Unité Mixte de Recherche CNRS-Université Paul Sabatier 5273, EFS, U1031 INSERM, BP 84225 31432 Toulouse Cedex 4, France,
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Alexandra Gouazé
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Xavier Fioramonti
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Xavier Brenachot
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Christophe Guissard
2STROMAlab; Unité Mixte de Recherche CNRS-Université Paul Sabatier 5273, EFS, U1031 INSERM, BP 84225 31432 Toulouse Cedex 4, France,
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Alice Krezymon
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Thibaut Duparc
3Institut des Maladies Métaboliques et Cardiovasculaires, Unité de Recherche 1048 INSERM, F-31432 Toulouse Cedex 4, France, and
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André Colom
3Institut des Maladies Métaboliques et Cardiovasculaires, Unité de Recherche 1048 INSERM, F-31432 Toulouse Cedex 4, France, and
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Emmanuelle Nédélec
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Caroline Rigault
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Aleth Lemoine
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Jean Gascuel
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Rita Gerardy-Schahn
4Institute for Cellular Chemistry, Hannover Medical School, 30625 Hannover, Germany
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Philippe Valet
3Institut des Maladies Métaboliques et Cardiovasculaires, Unité de Recherche 1048 INSERM, F-31432 Toulouse Cedex 4, France, and
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Claude Knauf
3Institut des Maladies Métaboliques et Cardiovasculaires, Unité de Recherche 1048 INSERM, F-31432 Toulouse Cedex 4, France, and
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Anne Lorsignol
2STROMAlab; Unité Mixte de Recherche CNRS-Université Paul Sabatier 5273, EFS, U1031 INSERM, BP 84225 31432 Toulouse Cedex 4, France,
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Luc Pénicaud
1Centre des Sciences du Goût et de l'Alimentation, Unité Mixte de Recherche 6265-CNRS, 1324-INRA, Université de Bourgogne, 21000 Dijon, France,
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Abstract

Hormones such as leptin and ghrelin can rapidly rewire hypothalamic feeding circuits when injected into rodent brains. These experimental manipulations suggest that the hypothalamus might reorganize continually in adulthood to integrate the metabolic status of the whole body. In this study, we examined whether hypothalamic plasticity occurs in naive animals according to their nutritional conditions. For this purpose, we fed mice with a short-term high-fat diet (HFD) and assessed brain remodeling through its molecular and functional signature. We found that HFD for 3 d rewired the hypothalamic arcuate nucleus, increasing the anorexigenic tone due to activated pro-opiomelanocortin (POMC) neurons. We identified the polysialic acid molecule (PSA) as a mediator of the diet-induced rewiring of arcuate POMC. Moreover, local pharmacological inhibition and genetic disruption of the PSA signaling limits the behavioral and metabolic adaptation to HFD, as treated mice failed to normalize energy intake and showed increased body weight gain after the HFD challenge. Altogether, these findings reveal the existence of physiological hypothalamic rewiring involved in the homeostatic response to dietary fat. Furthermore, defects in the hypothalamic plasticity-driven adaptive response to HFD are obesogenic and could be involved in the development of metabolic diseases.

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The Journal of Neuroscience: 32 (35)
Journal of Neuroscience
Vol. 32, Issue 35
29 Aug 2012
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Food Intake Adaptation to Dietary Fat Involves PSA-Dependent Rewiring of the Arcuate Melanocortin System in Mice
Alexandre Benani, Cécile Hryhorczuk, Alexandra Gouazé, Xavier Fioramonti, Xavier Brenachot, Christophe Guissard, Alice Krezymon, Thibaut Duparc, André Colom, Emmanuelle Nédélec, Caroline Rigault, Aleth Lemoine, Jean Gascuel, Rita Gerardy-Schahn, Philippe Valet, Claude Knauf, Anne Lorsignol, Luc Pénicaud
Journal of Neuroscience 29 August 2012, 32 (35) 11970-11979; DOI: 10.1523/JNEUROSCI.0624-12.2012

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Food Intake Adaptation to Dietary Fat Involves PSA-Dependent Rewiring of the Arcuate Melanocortin System in Mice
Alexandre Benani, Cécile Hryhorczuk, Alexandra Gouazé, Xavier Fioramonti, Xavier Brenachot, Christophe Guissard, Alice Krezymon, Thibaut Duparc, André Colom, Emmanuelle Nédélec, Caroline Rigault, Aleth Lemoine, Jean Gascuel, Rita Gerardy-Schahn, Philippe Valet, Claude Knauf, Anne Lorsignol, Luc Pénicaud
Journal of Neuroscience 29 August 2012, 32 (35) 11970-11979; DOI: 10.1523/JNEUROSCI.0624-12.2012
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