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Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life

Early in life and particularly around weaning, piglets are susceptible to infections because of abrupt social, environmental, and dietary changes. Dietary interventions with probiotic bacteria have gained popularity because of the increased awareness of the direct link between diet and health. In th...

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Autores principales: Geervliet, Mirelle, de Vries, Hugo, Jansen, Christine A., Rutten, Victor P. M. G., van Hees, Hubèrt, Wen, Caifang, Skovgaard, Kerstin, Antonello, Giacomo, Savelkoul, Huub F. J., Smidt, Hauke, Tijhaar, Edwin, Wells, Jerry M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8914288/
https://www.ncbi.nlm.nih.gov/pubmed/35283814
http://dx.doi.org/10.3389/fmicb.2022.842437
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author Geervliet, Mirelle
de Vries, Hugo
Jansen, Christine A.
Rutten, Victor P. M. G.
van Hees, Hubèrt
Wen, Caifang
Skovgaard, Kerstin
Antonello, Giacomo
Savelkoul, Huub F. J.
Smidt, Hauke
Tijhaar, Edwin
Wells, Jerry M.
author_facet Geervliet, Mirelle
de Vries, Hugo
Jansen, Christine A.
Rutten, Victor P. M. G.
van Hees, Hubèrt
Wen, Caifang
Skovgaard, Kerstin
Antonello, Giacomo
Savelkoul, Huub F. J.
Smidt, Hauke
Tijhaar, Edwin
Wells, Jerry M.
author_sort Geervliet, Mirelle
collection PubMed
description Early in life and particularly around weaning, piglets are susceptible to infections because of abrupt social, environmental, and dietary changes. Dietary interventions with probiotic bacteria have gained popularity because of the increased awareness of the direct link between diet and health. In this study, piglets received the probiotic strain Escherichia coli Nissle 1917 (EcN) or a control treatment perorally from day 2 after birth until 2 weeks post-weaning. To investigate spatio-temporal effects of EcN on the gut microbiota composition, intestinal epithelial gene expression and immune system, feces, digesta, blood, scraping material and mesenteric lymph node tissue were collected at different time points. In addition, oral vaccinations against Salmonella enterica serovar Typhimurium were administered on days 21 and 45 of the study to assess the immunocompetence. EcN-treated pigs showed a reduced diversity of taxa within the phylum Proteobacteria and a lower relative abundance of taxa within the genus Treponema during the pre-weaning period. Moreover, EcN induced T cell proliferation and Natural Killer cell activation in blood and enhanced IL-10 production in ex vivo stimulated mesenteric lymph node cells, the latter pointing toward a more regulatory or anti-inflammatory state of the local gut-associated immune system. These outcomes were primarily observed pre-weaning. No significant differences were observed between the treatment groups with regards to body weight, epithelial gene expression, and immune response upon vaccination. Differences observed during the post-weaning period between the treatment groups were modest. Overall, this study demonstrates that the pre-weaning period offers a ‘window of opportunity’ to modulate the porcine gut microbiota and immune system through dietary interventions such as EcN supplementation.
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spelling pubmed-89142882022-03-12 Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life Geervliet, Mirelle de Vries, Hugo Jansen, Christine A. Rutten, Victor P. M. G. van Hees, Hubèrt Wen, Caifang Skovgaard, Kerstin Antonello, Giacomo Savelkoul, Huub F. J. Smidt, Hauke Tijhaar, Edwin Wells, Jerry M. Front Microbiol Microbiology Early in life and particularly around weaning, piglets are susceptible to infections because of abrupt social, environmental, and dietary changes. Dietary interventions with probiotic bacteria have gained popularity because of the increased awareness of the direct link between diet and health. In this study, piglets received the probiotic strain Escherichia coli Nissle 1917 (EcN) or a control treatment perorally from day 2 after birth until 2 weeks post-weaning. To investigate spatio-temporal effects of EcN on the gut microbiota composition, intestinal epithelial gene expression and immune system, feces, digesta, blood, scraping material and mesenteric lymph node tissue were collected at different time points. In addition, oral vaccinations against Salmonella enterica serovar Typhimurium were administered on days 21 and 45 of the study to assess the immunocompetence. EcN-treated pigs showed a reduced diversity of taxa within the phylum Proteobacteria and a lower relative abundance of taxa within the genus Treponema during the pre-weaning period. Moreover, EcN induced T cell proliferation and Natural Killer cell activation in blood and enhanced IL-10 production in ex vivo stimulated mesenteric lymph node cells, the latter pointing toward a more regulatory or anti-inflammatory state of the local gut-associated immune system. These outcomes were primarily observed pre-weaning. No significant differences were observed between the treatment groups with regards to body weight, epithelial gene expression, and immune response upon vaccination. Differences observed during the post-weaning period between the treatment groups were modest. Overall, this study demonstrates that the pre-weaning period offers a ‘window of opportunity’ to modulate the porcine gut microbiota and immune system through dietary interventions such as EcN supplementation. Frontiers Media S.A. 2022-02-25 /pmc/articles/PMC8914288/ /pubmed/35283814 http://dx.doi.org/10.3389/fmicb.2022.842437 Text en Copyright © 2022 Geervliet, de Vries, Jansen, Rutten, van Hees, Wen, Skovgaard, Antonello, Savelkoul, Smidt, Tijhaar and Wells. https://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
Geervliet, Mirelle
de Vries, Hugo
Jansen, Christine A.
Rutten, Victor P. M. G.
van Hees, Hubèrt
Wen, Caifang
Skovgaard, Kerstin
Antonello, Giacomo
Savelkoul, Huub F. J.
Smidt, Hauke
Tijhaar, Edwin
Wells, Jerry M.
Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title_full Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title_fullStr Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title_full_unstemmed Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title_short Effects of Escherichia coli Nissle 1917 on the Porcine Gut Microbiota, Intestinal Epithelium and Immune System in Early Life
title_sort effects of escherichia coli nissle 1917 on the porcine gut microbiota, intestinal epithelium and immune system in early life
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8914288/
https://www.ncbi.nlm.nih.gov/pubmed/35283814
http://dx.doi.org/10.3389/fmicb.2022.842437
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