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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Main Authors: Xuan Li, Mingyu Mao, Yanan Zhang, Kaifan Yu, Weiyun Zhu
Format: Article
Language:English
Published: MDPI AG 2019-09-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/9/9/486
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author Xuan Li
Mingyu Mao
Yanan Zhang
Kaifan Yu
Weiyun Zhu
author_facet Xuan Li
Mingyu Mao
Yanan Zhang
Kaifan Yu
Weiyun Zhu
author_sort Xuan Li
collection DOAJ
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 (<i>n</i> = 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 doaj.art-38a5239297f94300bc539f05d288d2872022-12-21T19:49:19ZengMDPI AGBiomolecules2218-273X2019-09-019948610.3390/biom9090486biom9090486Succinate Modulates Intestinal Barrier Function and Inflammation Response in PigsXuan Li0Mingyu Mao1Yanan Zhang2Kaifan Yu3Weiyun Zhu4Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaSuccinate 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 (<i>n</i> = 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.https://www.mdpi.com/2218-273X/9/9/486succinateintestinal epithelial barrierintestinal inflammationpigs
spellingShingle Xuan Li
Mingyu Mao
Yanan Zhang
Kaifan Yu
Weiyun Zhu
Succinate Modulates Intestinal Barrier Function and Inflammation Response in Pigs
Biomolecules
succinate
intestinal epithelial barrier
intestinal inflammation
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 succinate
intestinal epithelial barrier
intestinal inflammation
pigs
url https://www.mdpi.com/2218-273X/9/9/486
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AT mingyumao succinatemodulatesintestinalbarrierfunctionandinflammationresponseinpigs
AT yananzhang succinatemodulatesintestinalbarrierfunctionandinflammationresponseinpigs
AT kaifanyu succinatemodulatesintestinalbarrierfunctionandinflammationresponseinpigs
AT weiyunzhu succinatemodulatesintestinalbarrierfunctionandinflammationresponseinpigs