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The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse

Dany Gaillard^*,1, Fabienne Laugerette^*,,1, Nicolas Darcel, Abdelghani El-Yassimi, Patricia Passilly-Degrace^*, Aziz Hichami, Naim Akhtar Khan, Jean-Pierre Montmayeur and Philippe Besnard^*,2

^* Physiologie de la Nutrition, UMR INSERM U 866, Ecole Nationale Supérieure de Biologie Appliquée à la Nutrition et à l’Alimentation, Université de Bourgogne, Dijon, France;

Chimioréception, Centre Européen des Sciences du Goût, UMR 5170 Centre National de la Recherche Scientifique/1214 Institut National de la Recherche Agronomique (INRA)/Université de Bourgogne, Dijon, France;

Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris Grignon (INAPG), UMR 914 INRA/INAPG, Paris, France; and

Unité Propre de Recherche de l’Enseignement Supérieur (UPRES) 4183 Lipides et Signalisation Cellulaire, Université de Bourgogne, Dijon, France

²Correspondence: Physiologie de la Nutrition, UMR INSERM U866, ENSBANA—Université de Bourgogne, 1, Esplanade Erasme F-21000, Dijon, France. E-mail: pbesnard{at}u-bourgogne.fr

The sense of taste informs the body about the quality of ingested foods. Tastant-mediated signals are generated by a rise in free intracellular calcium levels ([Ca²⁺]i) in the taste bud cells and then are transferred to the gustatory area of brain via connections between the gustatory nerves (chorda tympani and glossopharyngeal nerves) and the nucleus of solitary tract in the brain stem. We have recently shown that lingual CD36 contributes to fat preference and early digestive secretions in the mouse. We show here that 1) the induction of an increase in [Ca²⁺]i by linoleic acid is CD36-dependent in taste receptor cells, 2) the spontaneous preference for or conversely conditioned aversion to linoleic acid requires intact gustatory nerves, and 3) the activation of gustatory neurons in the nucleus of the solitary tract elicited by a linoleic acid deposition on the tongue in wild-type mice cannot be reproduced in CD36-null animals. We conclude that the CD36-mediated perception of long-chain fatty acids involves the gustatory pathway, suggesting that the mouse may have a "taste" for fatty foods. This system would constitute a potential physiological advantage under conditions of food scarcity by leading the mouse to select and absorb fatty foods. However, it might also lead to a risk of obesity and associated diseases in a context of constantly abundant food.—Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Passilly-Degrace, P., Hichami, A., Khan, N. A., Montmayeur, J.-P., Besnard, P. The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse.

Key Words: dietary lipid perception • gustation • feeding behavior • obesity risk