Patterns of early gut colonization shape future immune responses of the host.

The most important trigger for immune system development is the exposure to microbial components immediately after birth. Moreover, targeted manipulation of the microbiota can be used to change host susceptibility to immune-mediated diseases. Our aim was to analyze how differences in early gut colon...

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Autores principales: Camilla Hartmann Friis Hansen, Dennis Sandris Nielsen, Miloslav Kverka, Zuzana Zakostelska, Klara Klimesova, Tomas Hudcovic, Helena Tlaskalova-Hogenova, Axel Kornerup Hansen
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Publicado: Public Library of Science (PLoS) 2012
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spelling oai:doaj.org-article:8b4af3851f414b5f98bf3369f0d181242021-11-18T07:24:12ZPatterns of early gut colonization shape future immune responses of the host.1932-620310.1371/journal.pone.0034043https://doaj.org/article/8b4af3851f414b5f98bf3369f0d181242012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22479515/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203The most important trigger for immune system development is the exposure to microbial components immediately after birth. Moreover, targeted manipulation of the microbiota can be used to change host susceptibility to immune-mediated diseases. Our aim was to analyze how differences in early gut colonization patterns change the composition of the resident microbiota and future immune system reactivity. Germ-free (GF) mice were either inoculated by single oral gavage of caecal content or let colonized by co-housing with specific pathogen-free (SPF) mice at different time points in the postnatal period. The microbiota composition was analyzed by denaturing gradient gel electrophoresis for 16S rRNA gene followed by principal component analysis. Furthermore, immune functions and cytokine concentrations were analyzed using flow cytometry, ELISA or multiplex bead assay. We found that a single oral inoculation of GF mice at three weeks of age permanently changed the gut microbiota composition, which was not possible to achieve at one week of age. Interestingly, the ex-GF mice inoculated at three weeks of age were also the only mice with an increased pro-inflammatory immune response. In contrast, the composition of the gut microbiota of ex-GF mice that were co-housed with SPF mice at different time points was similar to the gut microbiota in the barrier maintained SPF mice. The existence of a short GF postnatal period permanently changed levels of systemic regulatory T cells, NK and NKT cells, and cytokine production. In conclusion, a time window exists that enables the artificial colonization of GF mice by a single oral dose of caecal content, which may modify the future immune phenotype of the host. Moreover, delayed microbial colonization of the gut causes permanent changes in the immune system.Camilla Hartmann Friis HansenDennis Sandris NielsenMiloslav KverkaZuzana ZakostelskaKlara KlimesovaTomas HudcovicHelena Tlaskalova-HogenovaAxel Kornerup HansenPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 3, p e34043 (2012)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Camilla Hartmann Friis Hansen
Dennis Sandris Nielsen
Miloslav Kverka
Zuzana Zakostelska
Klara Klimesova
Tomas Hudcovic
Helena Tlaskalova-Hogenova
Axel Kornerup Hansen
Patterns of early gut colonization shape future immune responses of the host.
description The most important trigger for immune system development is the exposure to microbial components immediately after birth. Moreover, targeted manipulation of the microbiota can be used to change host susceptibility to immune-mediated diseases. Our aim was to analyze how differences in early gut colonization patterns change the composition of the resident microbiota and future immune system reactivity. Germ-free (GF) mice were either inoculated by single oral gavage of caecal content or let colonized by co-housing with specific pathogen-free (SPF) mice at different time points in the postnatal period. The microbiota composition was analyzed by denaturing gradient gel electrophoresis for 16S rRNA gene followed by principal component analysis. Furthermore, immune functions and cytokine concentrations were analyzed using flow cytometry, ELISA or multiplex bead assay. We found that a single oral inoculation of GF mice at three weeks of age permanently changed the gut microbiota composition, which was not possible to achieve at one week of age. Interestingly, the ex-GF mice inoculated at three weeks of age were also the only mice with an increased pro-inflammatory immune response. In contrast, the composition of the gut microbiota of ex-GF mice that were co-housed with SPF mice at different time points was similar to the gut microbiota in the barrier maintained SPF mice. The existence of a short GF postnatal period permanently changed levels of systemic regulatory T cells, NK and NKT cells, and cytokine production. In conclusion, a time window exists that enables the artificial colonization of GF mice by a single oral dose of caecal content, which may modify the future immune phenotype of the host. Moreover, delayed microbial colonization of the gut causes permanent changes in the immune system.
format article
author Camilla Hartmann Friis Hansen
Dennis Sandris Nielsen
Miloslav Kverka
Zuzana Zakostelska
Klara Klimesova
Tomas Hudcovic
Helena Tlaskalova-Hogenova
Axel Kornerup Hansen
author_facet Camilla Hartmann Friis Hansen
Dennis Sandris Nielsen
Miloslav Kverka
Zuzana Zakostelska
Klara Klimesova
Tomas Hudcovic
Helena Tlaskalova-Hogenova
Axel Kornerup Hansen
author_sort Camilla Hartmann Friis Hansen
title Patterns of early gut colonization shape future immune responses of the host.
title_short Patterns of early gut colonization shape future immune responses of the host.
title_full Patterns of early gut colonization shape future immune responses of the host.
title_fullStr Patterns of early gut colonization shape future immune responses of the host.
title_full_unstemmed Patterns of early gut colonization shape future immune responses of the host.
title_sort patterns of early gut colonization shape future immune responses of the host.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/8b4af3851f414b5f98bf3369f0d18124
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