A glucokinase-linked sensor in the taste system contributes to glucose appetite

Objectives: Dietary glucose is a robust elicitor of central reward responses and ingestion, but the key peripheral sensors triggering these orexigenic mechanisms are not entirely known. The objective of this study was to determine whether glucokinase, a phosphorylating enzyme with known glucosensory...

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Main Authors: Sandrine Chometton, A-Hyun Jung, Lilly Mai, Taylor Dal Bon, Alexa Osorio Ramirez, David W. Pittman, Lindsey A. Schier
Format: Article
Language:English
Published: Elsevier 2022-10-01
Series:Molecular Metabolism
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2212877822001235
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author Sandrine Chometton
A-Hyun Jung
Lilly Mai
Taylor Dal Bon
Alexa Osorio Ramirez
David W. Pittman
Lindsey A. Schier
author_facet Sandrine Chometton
A-Hyun Jung
Lilly Mai
Taylor Dal Bon
Alexa Osorio Ramirez
David W. Pittman
Lindsey A. Schier
author_sort Sandrine Chometton
collection DOAJ
description Objectives: Dietary glucose is a robust elicitor of central reward responses and ingestion, but the key peripheral sensors triggering these orexigenic mechanisms are not entirely known. The objective of this study was to determine whether glucokinase, a phosphorylating enzyme with known glucosensory roles, is also expressed in taste bud cells and contributes to the immediate hedonic appeal of glucose-containing substances. Methods and results: Glucokinase (GCK) gene transcripts were localized in murine taste bud cells with RNAScope®, and GCK mRNA was found to be upregulated in the circumvallate taste papillae in response to fasting and after a period of dietary access to added simple sugars in mice, as determined with real time-qPCR. Pharmacological activation of glucokinase with Compound A increased primary taste nerve and licking responses for glucose but did not impact responsivity to fructose in naïve mice. Virogenetic silencing of glucokinase in the major taste fields attenuated glucose-stimulated licking, especially in mice that also lacked sweet receptors, but did not disrupt consummatory behaviors for fructose or the low-calorie sweetener, sucralose in sugar naïve mice. Knockdown of lingual glucokinase weakened the acquired preference for glucose over fructose in sugar-experienced mice in brief access taste tests. Conclusions: Collectively, our data establish that glucokinase contributes to glucose appetition at the very first site of nutrient detection, in the oral cavity. The findings expand our understanding of orosensory inputs underlying nutrition, metabolism, and food reward.
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spelling doaj.art-4da23900cc074a1e8bb9c7b678967b9a2022-12-22T01:44:15ZengElsevierMolecular Metabolism2212-87782022-10-0164101554A glucokinase-linked sensor in the taste system contributes to glucose appetiteSandrine Chometton0A-Hyun Jung1Lilly Mai2Taylor Dal Bon3Alexa Osorio Ramirez4David W. Pittman5Lindsey A. Schier6Department of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USADepartment of Psychology, Wofford College, Spartanburg, SC, 29303, USADepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USA; Corresponding author. 835 Bloom Walk University of Southern California Los Angeles, CA 90089, USA.Objectives: Dietary glucose is a robust elicitor of central reward responses and ingestion, but the key peripheral sensors triggering these orexigenic mechanisms are not entirely known. The objective of this study was to determine whether glucokinase, a phosphorylating enzyme with known glucosensory roles, is also expressed in taste bud cells and contributes to the immediate hedonic appeal of glucose-containing substances. Methods and results: Glucokinase (GCK) gene transcripts were localized in murine taste bud cells with RNAScope®, and GCK mRNA was found to be upregulated in the circumvallate taste papillae in response to fasting and after a period of dietary access to added simple sugars in mice, as determined with real time-qPCR. Pharmacological activation of glucokinase with Compound A increased primary taste nerve and licking responses for glucose but did not impact responsivity to fructose in naïve mice. Virogenetic silencing of glucokinase in the major taste fields attenuated glucose-stimulated licking, especially in mice that also lacked sweet receptors, but did not disrupt consummatory behaviors for fructose or the low-calorie sweetener, sucralose in sugar naïve mice. Knockdown of lingual glucokinase weakened the acquired preference for glucose over fructose in sugar-experienced mice in brief access taste tests. Conclusions: Collectively, our data establish that glucokinase contributes to glucose appetition at the very first site of nutrient detection, in the oral cavity. The findings expand our understanding of orosensory inputs underlying nutrition, metabolism, and food reward.http://www.sciencedirect.com/science/article/pii/S2212877822001235Sugar sensingNutrient assimilationMetabolismFood rewardGustationIngestive motivation
spellingShingle Sandrine Chometton
A-Hyun Jung
Lilly Mai
Taylor Dal Bon
Alexa Osorio Ramirez
David W. Pittman
Lindsey A. Schier
A glucokinase-linked sensor in the taste system contributes to glucose appetite
Molecular Metabolism
Sugar sensing
Nutrient assimilation
Metabolism
Food reward
Gustation
Ingestive motivation
title A glucokinase-linked sensor in the taste system contributes to glucose appetite
title_full A glucokinase-linked sensor in the taste system contributes to glucose appetite
title_fullStr A glucokinase-linked sensor in the taste system contributes to glucose appetite
title_full_unstemmed A glucokinase-linked sensor in the taste system contributes to glucose appetite
title_short A glucokinase-linked sensor in the taste system contributes to glucose appetite
title_sort glucokinase linked sensor in the taste system contributes to glucose appetite
topic Sugar sensing
Nutrient assimilation
Metabolism
Food reward
Gustation
Ingestive motivation
url http://www.sciencedirect.com/science/article/pii/S2212877822001235
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