Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets

Piglets are susceptible to weaning stress, which weakens the barrier and immune function of the intestinal mucosa, causes inflammation, and ultimately affects animal growth and development. Ellagic acid (EA) is a natural polyphenol dilactone with various biological functions. However, The mechanisms...

Full description

Bibliographic Details
Main Authors: Yujie Lu, Mingwei Zhao, Jiayuan Mo, Ganqiu Lan, Jing Liang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2022.980271/full
_version_ 1811184812329795584
author Yujie Lu
Mingwei Zhao
Jiayuan Mo
Ganqiu Lan
Jing Liang
author_facet Yujie Lu
Mingwei Zhao
Jiayuan Mo
Ganqiu Lan
Jing Liang
author_sort Yujie Lu
collection DOAJ
description Piglets are susceptible to weaning stress, which weakens the barrier and immune function of the intestinal mucosa, causes inflammation, and ultimately affects animal growth and development. Ellagic acid (EA) is a natural polyphenol dilactone with various biological functions. However, The mechanisms underlying the effects of EA on animal health are still poorly known. Herein, we examined whether dietary supplementation with EA has a positive effect on growth performance, intestinal health, immune response, microbiota, or inflammation in weaned piglets. Sixty weaned piglets (age, 30 days) were randomly divided into two groups: the control group (basic diet) and the test group (basic diet + 500 g/t EA). The pigs were fed for 40 days under the same feeding and management conditions, and the growth performance of each individual was measured. At the end of the feeding period, samples were collected from the small intestinal mucosa for further analysis. Using these tissues, the transcriptome sequences and intestinal microbial diversity were analyzed in both groups. An inflammation model using small intestinal mucosal epithelial cells (IPEC-J2) was also constructed. Dietary EA supplementation significantly increased the average daily weight gain (ADG) and reduced diarrhea rate and serum diamine oxidase (DAO) levels of weaned piglets. Transcriptome sequencing results revealed 401 differentially expressed genes in the jejunum mucosal tissue of pigs in the control and test groups. Of these, 163 genes were up-regulated and 238 were down-regulated. The down-regulated genes were significantly enriched in 10 pathways (false discovery rate < 0.05), including seven pathways related to immune response. The results of bacterial 16s rDNA sequencing show that EA affects the composition of the intestinal microbiota in the cecum and rectum, and reveal significant differences in the abundances of Prevotella_9, Lactobacillus delbrueckii, and Lactobacillus reuteri between the test and control groups (P < 0.05). Experiments using the inflammation model showed that certain doses of EA promote the proliferation of IPEC-J2 cells, increase the relative mRNA expression levels of tight junction-related proteins (ZO-1 and Occludin), improve the compactness of the intestine, reduce the expression of inflammatory factors TNF-α and IL-6, and significantly reduce LPS-induced inflammation in IPEC-J2 cells. In conclusion, we found for the first time that dietary supplementation of EA affects the gut immune response and promotes the beneficial gut microbiota in weaned piglets, reduces the occurrence of inflammatory responses, and thereby promotes the growth and intestinal health of piglets.
first_indexed 2024-04-11T13:19:52Z
format Article
id doaj.art-0ec8493a3046420fa2433131fd13266f
institution Directory Open Access Journal
issn 2297-1769
language English
last_indexed 2024-04-11T13:19:52Z
publishDate 2022-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Veterinary Science
spelling doaj.art-0ec8493a3046420fa2433131fd13266f2022-12-22T04:22:15ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692022-09-01910.3389/fvets.2022.980271980271Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned pigletsYujie Lu0Mingwei Zhao1Jiayuan Mo2Ganqiu Lan3Jing Liang4College of Animal Science and Technology, Guangxi University, Nanning, ChinaGuangxi Guiken Jinmao Animal Husbandry Co., Ltd., Nanning, ChinaCollege of Animal Science and Technology, Guangxi University, Nanning, ChinaCollege of Animal Science and Technology, Guangxi University, Nanning, ChinaCollege of Animal Science and Technology, Guangxi University, Nanning, ChinaPiglets are susceptible to weaning stress, which weakens the barrier and immune function of the intestinal mucosa, causes inflammation, and ultimately affects animal growth and development. Ellagic acid (EA) is a natural polyphenol dilactone with various biological functions. However, The mechanisms underlying the effects of EA on animal health are still poorly known. Herein, we examined whether dietary supplementation with EA has a positive effect on growth performance, intestinal health, immune response, microbiota, or inflammation in weaned piglets. Sixty weaned piglets (age, 30 days) were randomly divided into two groups: the control group (basic diet) and the test group (basic diet + 500 g/t EA). The pigs were fed for 40 days under the same feeding and management conditions, and the growth performance of each individual was measured. At the end of the feeding period, samples were collected from the small intestinal mucosa for further analysis. Using these tissues, the transcriptome sequences and intestinal microbial diversity were analyzed in both groups. An inflammation model using small intestinal mucosal epithelial cells (IPEC-J2) was also constructed. Dietary EA supplementation significantly increased the average daily weight gain (ADG) and reduced diarrhea rate and serum diamine oxidase (DAO) levels of weaned piglets. Transcriptome sequencing results revealed 401 differentially expressed genes in the jejunum mucosal tissue of pigs in the control and test groups. Of these, 163 genes were up-regulated and 238 were down-regulated. The down-regulated genes were significantly enriched in 10 pathways (false discovery rate < 0.05), including seven pathways related to immune response. The results of bacterial 16s rDNA sequencing show that EA affects the composition of the intestinal microbiota in the cecum and rectum, and reveal significant differences in the abundances of Prevotella_9, Lactobacillus delbrueckii, and Lactobacillus reuteri between the test and control groups (P < 0.05). Experiments using the inflammation model showed that certain doses of EA promote the proliferation of IPEC-J2 cells, increase the relative mRNA expression levels of tight junction-related proteins (ZO-1 and Occludin), improve the compactness of the intestine, reduce the expression of inflammatory factors TNF-α and IL-6, and significantly reduce LPS-induced inflammation in IPEC-J2 cells. In conclusion, we found for the first time that dietary supplementation of EA affects the gut immune response and promotes the beneficial gut microbiota in weaned piglets, reduces the occurrence of inflammatory responses, and thereby promotes the growth and intestinal health of piglets.https://www.frontiersin.org/articles/10.3389/fvets.2022.980271/fullellagic acidintestinal mucosaimmune responseinflammationpig
spellingShingle Yujie Lu
Mingwei Zhao
Jiayuan Mo
Ganqiu Lan
Jing Liang
Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
Frontiers in Veterinary Science
ellagic acid
intestinal mucosa
immune response
inflammation
pig
title Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
title_full Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
title_fullStr Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
title_full_unstemmed Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
title_short Dietary supplementation ellagic acid on the growth, intestinal immune response, microbiota, and inflammation in weaned piglets
title_sort dietary supplementation ellagic acid on the growth intestinal immune response microbiota and inflammation in weaned piglets
topic ellagic acid
intestinal mucosa
immune response
inflammation
pig
url https://www.frontiersin.org/articles/10.3389/fvets.2022.980271/full
work_keys_str_mv AT yujielu dietarysupplementationellagicacidonthegrowthintestinalimmuneresponsemicrobiotaandinflammationinweanedpiglets
AT mingweizhao dietarysupplementationellagicacidonthegrowthintestinalimmuneresponsemicrobiotaandinflammationinweanedpiglets
AT jiayuanmo dietarysupplementationellagicacidonthegrowthintestinalimmuneresponsemicrobiotaandinflammationinweanedpiglets
AT ganqiulan dietarysupplementationellagicacidonthegrowthintestinalimmuneresponsemicrobiotaandinflammationinweanedpiglets
AT jingliang dietarysupplementationellagicacidonthegrowthintestinalimmuneresponsemicrobiotaandinflammationinweanedpiglets