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Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs

Succinate is a metabolic intermediate of the tricarboxylic acid (TCA) cycle in all aerobic organisms, and is also a vital microbial metabolite in the gut. Although succinate is known to regulate intestinal metabolism and immune function, its role in the protection of the intestinal epithelial barrie...

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Autores principales: Li, Xuan, Mao, Mingyu, Zhang, Yanan, Yu, Kaifan, Zhu, Weiyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6770553/
https://www.ncbi.nlm.nih.gov/pubmed/31540325
http://dx.doi.org/10.3390/biom9090486
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author Li, Xuan
Mao, Mingyu
Zhang, Yanan
Yu, Kaifan
Zhu, Weiyun
author_facet Li, Xuan
Mao, Mingyu
Zhang, Yanan
Yu, Kaifan
Zhu, Weiyun
author_sort Li, Xuan
collection PubMed
description Succinate is a metabolic intermediate of the tricarboxylic acid (TCA) cycle in all aerobic organisms, and is also a vital microbial metabolite in the gut. Although succinate is known to regulate intestinal metabolism and immune function, its role in the protection of the intestinal epithelial barrier function and inflammation is poorly characterized. In this study, we evaluated the effects of succinate on intestinal epithelial barrier function and inflammation in pigs. Twenty-four growing pigs were distributed into three groups (n = 8) and received either a basal diet (control group) or the same diet supplemented with 0.1% succinate or 1% succinate. The diet supplemented with 1% succinate led to alterations in the intestinal morphology. We confirmed in vitro that 5 mM succinate treatment modulated intestinal epithelial permeability by increased transepithelial electrical resistance (TEER) in intestinal porcine epithelial cell (IPEC)-J2 cells. Furthermore, succinate treatment increased the abundance of tight junction proteins claudin-1, zona occluden (ZO)-1, and ZO-2 in the jejunum in vivo and in vitro. In addition, dietary succinate supplementation promoted the expression of inflammatory cytokines interleukin (IL)-25, IL-10, IL-8, and IL-18 in the jejunum. Taken together, these data identify a novel role of succinate in the modulation of intestinal epithelial barrier function, which may be a nutritional target to improve gut health in animals.
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spelling pubmed-67705532019-10-30 Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs Li, Xuan Mao, Mingyu Zhang, Yanan Yu, Kaifan Zhu, Weiyun Biomolecules Article Succinate is a metabolic intermediate of the tricarboxylic acid (TCA) cycle in all aerobic organisms, and is also a vital microbial metabolite in the gut. Although succinate is known to regulate intestinal metabolism and immune function, its role in the protection of the intestinal epithelial barrier function and inflammation is poorly characterized. In this study, we evaluated the effects of succinate on intestinal epithelial barrier function and inflammation in pigs. Twenty-four growing pigs were distributed into three groups (n = 8) and received either a basal diet (control group) or the same diet supplemented with 0.1% succinate or 1% succinate. The diet supplemented with 1% succinate led to alterations in the intestinal morphology. We confirmed in vitro that 5 mM succinate treatment modulated intestinal epithelial permeability by increased transepithelial electrical resistance (TEER) in intestinal porcine epithelial cell (IPEC)-J2 cells. Furthermore, succinate treatment increased the abundance of tight junction proteins claudin-1, zona occluden (ZO)-1, and ZO-2 in the jejunum in vivo and in vitro. In addition, dietary succinate supplementation promoted the expression of inflammatory cytokines interleukin (IL)-25, IL-10, IL-8, and IL-18 in the jejunum. Taken together, these data identify a novel role of succinate in the modulation of intestinal epithelial barrier function, which may be a nutritional target to improve gut health in animals. MDPI 2019-09-13 /pmc/articles/PMC6770553/ /pubmed/31540325 http://dx.doi.org/10.3390/biom9090486 Text en © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Li, Xuan
Mao, Mingyu
Zhang, Yanan
Yu, Kaifan
Zhu, Weiyun
Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title_full Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title_fullStr Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title_full_unstemmed Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title_short Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
title_sort succinate modulates intestinal barrier function and inflammation response in pigs
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6770553/
https://www.ncbi.nlm.nih.gov/pubmed/31540325
http://dx.doi.org/10.3390/biom9090486
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