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Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet

AIM: The tools that have been used to assess the function of the vagus nerve lack specificity. This could explain discrepancies about the role of vagal gut‐brain signalling in long‐term control of energy balance. Here we use a validated approach to selectively ablate sensory vagal neurones that inne...

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Autores principales: McDougle, Molly, Quinn, Danielle, Diepenbroek, Charlene, Singh, Arashdeep, de la Serre, Claire, de Lartigue, Guillaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7772266/
https://www.ncbi.nlm.nih.gov/pubmed/32603548
http://dx.doi.org/10.1111/apha.13530
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author McDougle, Molly
Quinn, Danielle
Diepenbroek, Charlene
Singh, Arashdeep
de la Serre, Claire
de Lartigue, Guillaume
author_facet McDougle, Molly
Quinn, Danielle
Diepenbroek, Charlene
Singh, Arashdeep
de la Serre, Claire
de Lartigue, Guillaume
author_sort McDougle, Molly
collection PubMed
description AIM: The tools that have been used to assess the function of the vagus nerve lack specificity. This could explain discrepancies about the role of vagal gut‐brain signalling in long‐term control of energy balance. Here we use a validated approach to selectively ablate sensory vagal neurones that innervate the gut to determine the role of vagal gut‐brain signalling in the control of food intake, energy expenditure and glucose homoeostasis in response to different diets. METHODS: Rat nodose ganglia were injected bilaterally with either the neurotoxin saporin conjugated to the gastrointestinal hormone cholecystokinin (CCK), or unconjugated saporin as a control. Food intake, body weight, glucose tolerance and energy expenditure were measured in both groups in response to chow or high‐fat high‐sugar (HFHS) diet. Willingness to work for fat or sugar was assessed by progressive ratio for orally administered solutions, while post‐ingestive feedback was tested by measuring food intake after an isocaloric lipid or sucrose pre‐load. RESULTS: Vagal deafferentation of the gut increases meal number in lean chow‐fed rats. Switching to a HFHS diet exacerbates overeating and body weight gain. The breakpoint for sugar or fat solution did not differ between groups, suggesting that increased palatability may not drive HFHS‐induced hyperphagia. Instead, decreased satiation in response to intra‐gastric infusion of fat, but not sugar, promotes hyperphagia in CCK‐Saporin‐treated rats fed with HFHS diet. CONCLUSIONS: We conclude that intact sensory vagal neurones prevent hyperphagia and exacerbation of weight gain in response to a HFHS diet by promoting lipid‐mediated satiation.
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spelling pubmed-77722662021-03-25 Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet McDougle, Molly Quinn, Danielle Diepenbroek, Charlene Singh, Arashdeep de la Serre, Claire de Lartigue, Guillaume Acta Physiol (Oxf) Metabolism and Nutritional Physiology AIM: The tools that have been used to assess the function of the vagus nerve lack specificity. This could explain discrepancies about the role of vagal gut‐brain signalling in long‐term control of energy balance. Here we use a validated approach to selectively ablate sensory vagal neurones that innervate the gut to determine the role of vagal gut‐brain signalling in the control of food intake, energy expenditure and glucose homoeostasis in response to different diets. METHODS: Rat nodose ganglia were injected bilaterally with either the neurotoxin saporin conjugated to the gastrointestinal hormone cholecystokinin (CCK), or unconjugated saporin as a control. Food intake, body weight, glucose tolerance and energy expenditure were measured in both groups in response to chow or high‐fat high‐sugar (HFHS) diet. Willingness to work for fat or sugar was assessed by progressive ratio for orally administered solutions, while post‐ingestive feedback was tested by measuring food intake after an isocaloric lipid or sucrose pre‐load. RESULTS: Vagal deafferentation of the gut increases meal number in lean chow‐fed rats. Switching to a HFHS diet exacerbates overeating and body weight gain. The breakpoint for sugar or fat solution did not differ between groups, suggesting that increased palatability may not drive HFHS‐induced hyperphagia. Instead, decreased satiation in response to intra‐gastric infusion of fat, but not sugar, promotes hyperphagia in CCK‐Saporin‐treated rats fed with HFHS diet. CONCLUSIONS: We conclude that intact sensory vagal neurones prevent hyperphagia and exacerbation of weight gain in response to a HFHS diet by promoting lipid‐mediated satiation. John Wiley and Sons Inc. 2020-07-22 2021-03 /pmc/articles/PMC7772266/ /pubmed/32603548 http://dx.doi.org/10.1111/apha.13530 Text en © 2020 The Authors. Acta Physiologica published by John Wiley & Sons Ltd on behalf of Scandinavian Physiological Society This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Metabolism and Nutritional Physiology
McDougle, Molly
Quinn, Danielle
Diepenbroek, Charlene
Singh, Arashdeep
de la Serre, Claire
de Lartigue, Guillaume
Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title_full Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title_fullStr Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title_full_unstemmed Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title_short Intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
title_sort intact vagal gut‐brain signalling prevents hyperphagia and excessive weight gain in response to high‐fat high‐sugar diet
topic Metabolism and Nutritional Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7772266/
https://www.ncbi.nlm.nih.gov/pubmed/32603548
http://dx.doi.org/10.1111/apha.13530
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