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TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling

Cholinergic and sympathetic counter-regulatory networks control numerous physiological functions, including learning/memory/cognition, stress responsiveness, blood pressure, heart rate, and energy balance. As neurons primarily utilize glucose as their primary metabolic energy source, we generated mi...

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Autores principales: Tang, Yan, Zong, Haihong, Kwon, Hyokjoon, Qiu, Yunping, Pessin, Jacob B, Wu, Licheng, Buddo, Katherine A, Boykov, Ilya, Schmidt, Cameron A, Lin, Chien-Te, Neufer, P Darrell, Schwartz, Gary J, Kurland, Irwin J, Pessin, Jeffrey E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947760/
https://www.ncbi.nlm.nih.gov/pubmed/35254259
http://dx.doi.org/10.7554/eLife.73360
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author Tang, Yan
Zong, Haihong
Kwon, Hyokjoon
Qiu, Yunping
Pessin, Jacob B
Wu, Licheng
Buddo, Katherine A
Boykov, Ilya
Schmidt, Cameron A
Lin, Chien-Te
Neufer, P Darrell
Schwartz, Gary J
Kurland, Irwin J
Pessin, Jeffrey E
author_facet Tang, Yan
Zong, Haihong
Kwon, Hyokjoon
Qiu, Yunping
Pessin, Jacob B
Wu, Licheng
Buddo, Katherine A
Boykov, Ilya
Schmidt, Cameron A
Lin, Chien-Te
Neufer, P Darrell
Schwartz, Gary J
Kurland, Irwin J
Pessin, Jeffrey E
author_sort Tang, Yan
collection PubMed
description Cholinergic and sympathetic counter-regulatory networks control numerous physiological functions, including learning/memory/cognition, stress responsiveness, blood pressure, heart rate, and energy balance. As neurons primarily utilize glucose as their primary metabolic energy source, we generated mice with increased glycolysis in cholinergic neurons by specific deletion of the fructose-2,6-phosphatase protein TIGAR. Steady-state and stable isotope flux analyses demonstrated increased rates of glycolysis, acetyl-CoA production, acetylcholine levels, and density of neuromuscular synaptic junction clusters with enhanced acetylcholine release. The increase in cholinergic signaling reduced blood pressure and heart rate with a remarkable resistance to cold-induced hypothermia. These data directly demonstrate that increased cholinergic signaling through the modulation of glycolysis has several metabolic benefits particularly to increase energy expenditure and heat production upon cold exposure.
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spelling pubmed-89477602022-03-25 TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling Tang, Yan Zong, Haihong Kwon, Hyokjoon Qiu, Yunping Pessin, Jacob B Wu, Licheng Buddo, Katherine A Boykov, Ilya Schmidt, Cameron A Lin, Chien-Te Neufer, P Darrell Schwartz, Gary J Kurland, Irwin J Pessin, Jeffrey E eLife Cell Biology Cholinergic and sympathetic counter-regulatory networks control numerous physiological functions, including learning/memory/cognition, stress responsiveness, blood pressure, heart rate, and energy balance. As neurons primarily utilize glucose as their primary metabolic energy source, we generated mice with increased glycolysis in cholinergic neurons by specific deletion of the fructose-2,6-phosphatase protein TIGAR. Steady-state and stable isotope flux analyses demonstrated increased rates of glycolysis, acetyl-CoA production, acetylcholine levels, and density of neuromuscular synaptic junction clusters with enhanced acetylcholine release. The increase in cholinergic signaling reduced blood pressure and heart rate with a remarkable resistance to cold-induced hypothermia. These data directly demonstrate that increased cholinergic signaling through the modulation of glycolysis has several metabolic benefits particularly to increase energy expenditure and heat production upon cold exposure. eLife Sciences Publications, Ltd 2022-03-07 /pmc/articles/PMC8947760/ /pubmed/35254259 http://dx.doi.org/10.7554/eLife.73360 Text en © 2022, Tang et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Tang, Yan
Zong, Haihong
Kwon, Hyokjoon
Qiu, Yunping
Pessin, Jacob B
Wu, Licheng
Buddo, Katherine A
Boykov, Ilya
Schmidt, Cameron A
Lin, Chien-Te
Neufer, P Darrell
Schwartz, Gary J
Kurland, Irwin J
Pessin, Jeffrey E
TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title_full TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title_fullStr TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title_full_unstemmed TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title_short TIGAR deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
title_sort tigar deficiency enhances skeletal muscle thermogenesis by increasing neuromuscular junction cholinergic signaling
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947760/
https://www.ncbi.nlm.nih.gov/pubmed/35254259
http://dx.doi.org/10.7554/eLife.73360
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