Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.

<h4>Background</h4>Acquisition of the intestinal microbiota in early life corresponds with the development of the mucosal immune system. Recent work on caesarean-delivered infants revealed that early microbial composition is influenced by birthing method and environment. Furthermore, we...

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Autores principales:	Imke E Mulder, Bettina Schmidt, Marie Lewis, Margaret Delday, Christopher R Stokes, Mick Bailey, Rustam I Aminov, Bhupinder P Gill, John R Pluske, Claus-Dieter Mayer, Denise Kelly
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/55aaeb5944684f6f986190b6037c9a35
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spelling	oai:doaj.org-article:55aaeb5944684f6f986190b6037c9a352021-11-18T07:31:39ZRestricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.1932-620310.1371/journal.pone.0028279https://doaj.org/article/55aaeb5944684f6f986190b6037c9a352011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22216092/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Acquisition of the intestinal microbiota in early life corresponds with the development of the mucosal immune system. Recent work on caesarean-delivered infants revealed that early microbial composition is influenced by birthing method and environment. Furthermore, we have confirmed that early-life environment strongly influences both the adult gut microbiota and development of the gut immune system. Here, we address the impact of limiting microbial exposure after initial colonization on the development of adult gut immunity.<h4>Methodology/principal findings</h4>Piglets were born in indoor or outdoor rearing units, allowing natural colonization in the immediate period after birth, prior to transfer to high-health status isolators. Strikingly, gut closure and morphological development were strongly affected by isolator-rearing, independent of indoor or outdoor origins of piglets. Isolator-reared animals showed extensive vacuolation and disorganization of the gut epithelium, inferring that normal gut closure requires maturation factors present in maternal milk. Although morphological maturation and gut closure were delayed in isolator-reared animals, these hard-wired events occurred later in development. Type I IFN, IL-22, IL-23 and Th17 pathways were increased in indoor-isolator compared to outdoor-isolator animals during early life, indicating greater immune activation in pigs originating from indoor environments reflecting differences in the early microbiota. This difference was less apparent later in development due to enhanced immune activation and convergence of the microbiota in all isolator-reared animals. This correlated with elevation of Type I IFN pathways in both groups, although T cell pathways were still more affected in indoor-reared animals.<h4>Conclusions/significance</h4>Environmental factors, in particular microbial exposure, influence expression of a large number of immune-related genes. However, the homeostatic effects of microbial colonization in outdoor environments require sustained microbial exposure throughout development. Gut development in high-hygiene environments negatively impacts on normal succession of the gut microbiota and promotes innate immune activation which may impair immune homeostasis.Imke E MulderBettina SchmidtMarie LewisMargaret DeldayChristopher R StokesMick BaileyRustam I AminovBhupinder P GillJohn R PluskeClaus-Dieter MayerDenise KellyPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 12, p e28279 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Imke E Mulder Bettina Schmidt Marie Lewis Margaret Delday Christopher R Stokes Mick Bailey Rustam I Aminov Bhupinder P Gill John R Pluske Claus-Dieter Mayer Denise Kelly Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
description	<h4>Background</h4>Acquisition of the intestinal microbiota in early life corresponds with the development of the mucosal immune system. Recent work on caesarean-delivered infants revealed that early microbial composition is influenced by birthing method and environment. Furthermore, we have confirmed that early-life environment strongly influences both the adult gut microbiota and development of the gut immune system. Here, we address the impact of limiting microbial exposure after initial colonization on the development of adult gut immunity.<h4>Methodology/principal findings</h4>Piglets were born in indoor or outdoor rearing units, allowing natural colonization in the immediate period after birth, prior to transfer to high-health status isolators. Strikingly, gut closure and morphological development were strongly affected by isolator-rearing, independent of indoor or outdoor origins of piglets. Isolator-reared animals showed extensive vacuolation and disorganization of the gut epithelium, inferring that normal gut closure requires maturation factors present in maternal milk. Although morphological maturation and gut closure were delayed in isolator-reared animals, these hard-wired events occurred later in development. Type I IFN, IL-22, IL-23 and Th17 pathways were increased in indoor-isolator compared to outdoor-isolator animals during early life, indicating greater immune activation in pigs originating from indoor environments reflecting differences in the early microbiota. This difference was less apparent later in development due to enhanced immune activation and convergence of the microbiota in all isolator-reared animals. This correlated with elevation of Type I IFN pathways in both groups, although T cell pathways were still more affected in indoor-reared animals.<h4>Conclusions/significance</h4>Environmental factors, in particular microbial exposure, influence expression of a large number of immune-related genes. However, the homeostatic effects of microbial colonization in outdoor environments require sustained microbial exposure throughout development. Gut development in high-hygiene environments negatively impacts on normal succession of the gut microbiota and promotes innate immune activation which may impair immune homeostasis.
format	article
author	Imke E Mulder Bettina Schmidt Marie Lewis Margaret Delday Christopher R Stokes Mick Bailey Rustam I Aminov Bhupinder P Gill John R Pluske Claus-Dieter Mayer Denise Kelly
author_facet	Imke E Mulder Bettina Schmidt Marie Lewis Margaret Delday Christopher R Stokes Mick Bailey Rustam I Aminov Bhupinder P Gill John R Pluske Claus-Dieter Mayer Denise Kelly
author_sort	Imke E Mulder
title	Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
title_short	Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
title_full	Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
title_fullStr	Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
title_full_unstemmed	Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
title_sort	restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/55aaeb5944684f6f986190b6037c9a35
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Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity.

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