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Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage

Microbe-derived butyrate plays an important role in the gut health of young mammals during the weaning stage. A greater understanding of how butyrate regulates intestinal development is necessary for overcoming post-weaning diarrheal diseases. We aimed to investigate whether jejunal microbial metabo...

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Autores principales: Zhong, Xi, Zhang, Zhongwei, Wang, Shujin, Cao, Lili, Zhou, Lin, Sun, Aomin, Zhong, Zhendong, Nabben, Miranda
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345722/
https://www.ncbi.nlm.nih.gov/pubmed/30713531
http://dx.doi.org/10.3389/fmicb.2018.03335
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author Zhong, Xi
Zhang, Zhongwei
Wang, Shujin
Cao, Lili
Zhou, Lin
Sun, Aomin
Zhong, Zhendong
Nabben, Miranda
author_facet Zhong, Xi
Zhang, Zhongwei
Wang, Shujin
Cao, Lili
Zhou, Lin
Sun, Aomin
Zhong, Zhendong
Nabben, Miranda
author_sort Zhong, Xi
collection PubMed
description Microbe-derived butyrate plays an important role in the gut health of young mammals during the weaning stage. A greater understanding of how butyrate regulates intestinal development is necessary for overcoming post-weaning diarrheal diseases. We aimed to investigate whether jejunal microbial metabolite butyrate modulates the apoptosis/proliferation balance and immune response in piglets during the post-weaning period of the first 3 weeks of life. On the one hand, during the first week post-weaning, the relative abundances of the dominant bacterial families Erysipelotrichaceae (P < 0.01) and Lachnospiraceae (P < 0.01) were increased, which induced decreases in both butyrate production (P < 0.05) and its receptor (G-protein coupled receptor 43) expression (P < 0.01). The resulting intestinal inflammation (inferred from increased TNF-α and IFN-γ expression) contributed to the onset of cell apoptosis and the inhibition of cell-proliferation along the crypt-villus axis, which were followed by impaired jejunal morphology (i.e., increased crypt-depth) (P < 0.05) and intestinal dysfunction (i.e., decreased creatine kinase, and lactate dehydrogenase) (P < 0.05). On the other hand, during the second week post-weaning, the relative abundances of Lactobacillaceae (P < 0.01) and Ruminococcaceae (P < 0.05) were increased. The increases were accompanied by increased butyrate production (P < 0.05) and its receptor expression (P < 0.01), leading to the inhibition of cell apoptosis and the stimulation of cell proliferation via decreased pro-inflammatory cytokines and thereby the improvement of intestinal development and function. Herein, this study demonstrates that microbial-driven butyrate might be a key modulator in the maintenance of intestinal homeostasis after weaning. The findings suggest that strategies to promote butyrate production can maintain the apoptosis/proliferation balance via minimizing intestinal inflammation, and thereby improving post-weaning jejunal adaptation toward gut health.
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spelling pubmed-63457222019-02-01 Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage Zhong, Xi Zhang, Zhongwei Wang, Shujin Cao, Lili Zhou, Lin Sun, Aomin Zhong, Zhendong Nabben, Miranda Front Microbiol Microbiology Microbe-derived butyrate plays an important role in the gut health of young mammals during the weaning stage. A greater understanding of how butyrate regulates intestinal development is necessary for overcoming post-weaning diarrheal diseases. We aimed to investigate whether jejunal microbial metabolite butyrate modulates the apoptosis/proliferation balance and immune response in piglets during the post-weaning period of the first 3 weeks of life. On the one hand, during the first week post-weaning, the relative abundances of the dominant bacterial families Erysipelotrichaceae (P < 0.01) and Lachnospiraceae (P < 0.01) were increased, which induced decreases in both butyrate production (P < 0.05) and its receptor (G-protein coupled receptor 43) expression (P < 0.01). The resulting intestinal inflammation (inferred from increased TNF-α and IFN-γ expression) contributed to the onset of cell apoptosis and the inhibition of cell-proliferation along the crypt-villus axis, which were followed by impaired jejunal morphology (i.e., increased crypt-depth) (P < 0.05) and intestinal dysfunction (i.e., decreased creatine kinase, and lactate dehydrogenase) (P < 0.05). On the other hand, during the second week post-weaning, the relative abundances of Lactobacillaceae (P < 0.01) and Ruminococcaceae (P < 0.05) were increased. The increases were accompanied by increased butyrate production (P < 0.05) and its receptor expression (P < 0.01), leading to the inhibition of cell apoptosis and the stimulation of cell proliferation via decreased pro-inflammatory cytokines and thereby the improvement of intestinal development and function. Herein, this study demonstrates that microbial-driven butyrate might be a key modulator in the maintenance of intestinal homeostasis after weaning. The findings suggest that strategies to promote butyrate production can maintain the apoptosis/proliferation balance via minimizing intestinal inflammation, and thereby improving post-weaning jejunal adaptation toward gut health. Frontiers Media S.A. 2019-01-18 /pmc/articles/PMC6345722/ /pubmed/30713531 http://dx.doi.org/10.3389/fmicb.2018.03335 Text en Copyright © 2019 Zhong, Zhang, Wang, Cao, Zhou, Sun, Zhong and Nabben. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Zhong, Xi
Zhang, Zhongwei
Wang, Shujin
Cao, Lili
Zhou, Lin
Sun, Aomin
Zhong, Zhendong
Nabben, Miranda
Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title_full Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title_fullStr Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title_full_unstemmed Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title_short Microbial-Driven Butyrate Regulates Jejunal Homeostasis in Piglets During the Weaning Stage
title_sort microbial-driven butyrate regulates jejunal homeostasis in piglets during the weaning stage
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345722/
https://www.ncbi.nlm.nih.gov/pubmed/30713531
http://dx.doi.org/10.3389/fmicb.2018.03335
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