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Microbial regulation of intestinal motility provides resistance against helminth infection

Soil-transmitted helminths cause widespread disease, infecting ~1.5 billion people living within poverty-stricken regions of tropical and subtropical countries. As adult worms inhabit the intestine alongside bacterial communities, we determined whether the bacterial microbiota impacted on host resis...

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Autores principales: Moyat, Mati, Lebon, Luc, Perdijk, Olaf, Wickramasinghe, Lakshanie C., Zaiss, Mario M., Mosconi, Ilaria, Volpe, Beatrice, Guenat, Nadine, Shah, Kathleen, Coakley, Gillian, Bouchery, Tiffany, Harris, Nicola L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group US 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9705251/
https://www.ncbi.nlm.nih.gov/pubmed/35288644
http://dx.doi.org/10.1038/s41385-022-00498-8
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author Moyat, Mati
Lebon, Luc
Perdijk, Olaf
Wickramasinghe, Lakshanie C.
Zaiss, Mario M.
Mosconi, Ilaria
Volpe, Beatrice
Guenat, Nadine
Shah, Kathleen
Coakley, Gillian
Bouchery, Tiffany
Harris, Nicola L.
author_facet Moyat, Mati
Lebon, Luc
Perdijk, Olaf
Wickramasinghe, Lakshanie C.
Zaiss, Mario M.
Mosconi, Ilaria
Volpe, Beatrice
Guenat, Nadine
Shah, Kathleen
Coakley, Gillian
Bouchery, Tiffany
Harris, Nicola L.
author_sort Moyat, Mati
collection PubMed
description Soil-transmitted helminths cause widespread disease, infecting ~1.5 billion people living within poverty-stricken regions of tropical and subtropical countries. As adult worms inhabit the intestine alongside bacterial communities, we determined whether the bacterial microbiota impacted on host resistance against intestinal helminth infection. We infected germ-free, antibiotic-treated and specific pathogen-free mice, with the intestinal helminth Heligmosomoides polygyrus bakeri. Mice harboured increased parasite numbers in the absence of a bacterial microbiota, despite mounting a robust helminth-induced type 2 immune response. Alterations to parasite behaviour could already be observed at early time points following infection, including more proximal distribution of infective larvae along the intestinal tract and increased migration in a Baermann assay. Mice lacking a complex bacterial microbiota exhibited reduced levels of intestinal acetylcholine, a major excitatory intestinal neurotransmitter that promotes intestinal transit by activating muscarinic receptors. Both intestinal motility and host resistance against larval infection were restored by treatment with the muscarinic agonist bethanechol. These data provide evidence that a complex bacterial microbiota provides the host with resistance against intestinal helminths via its ability to regulate intestinal motility.
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spelling pubmed-97052512022-11-30 Microbial regulation of intestinal motility provides resistance against helminth infection Moyat, Mati Lebon, Luc Perdijk, Olaf Wickramasinghe, Lakshanie C. Zaiss, Mario M. Mosconi, Ilaria Volpe, Beatrice Guenat, Nadine Shah, Kathleen Coakley, Gillian Bouchery, Tiffany Harris, Nicola L. Mucosal Immunol Article Soil-transmitted helminths cause widespread disease, infecting ~1.5 billion people living within poverty-stricken regions of tropical and subtropical countries. As adult worms inhabit the intestine alongside bacterial communities, we determined whether the bacterial microbiota impacted on host resistance against intestinal helminth infection. We infected germ-free, antibiotic-treated and specific pathogen-free mice, with the intestinal helminth Heligmosomoides polygyrus bakeri. Mice harboured increased parasite numbers in the absence of a bacterial microbiota, despite mounting a robust helminth-induced type 2 immune response. Alterations to parasite behaviour could already be observed at early time points following infection, including more proximal distribution of infective larvae along the intestinal tract and increased migration in a Baermann assay. Mice lacking a complex bacterial microbiota exhibited reduced levels of intestinal acetylcholine, a major excitatory intestinal neurotransmitter that promotes intestinal transit by activating muscarinic receptors. Both intestinal motility and host resistance against larval infection were restored by treatment with the muscarinic agonist bethanechol. These data provide evidence that a complex bacterial microbiota provides the host with resistance against intestinal helminths via its ability to regulate intestinal motility. Nature Publishing Group US 2022-03-14 2022 /pmc/articles/PMC9705251/ /pubmed/35288644 http://dx.doi.org/10.1038/s41385-022-00498-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Moyat, Mati
Lebon, Luc
Perdijk, Olaf
Wickramasinghe, Lakshanie C.
Zaiss, Mario M.
Mosconi, Ilaria
Volpe, Beatrice
Guenat, Nadine
Shah, Kathleen
Coakley, Gillian
Bouchery, Tiffany
Harris, Nicola L.
Microbial regulation of intestinal motility provides resistance against helminth infection
title Microbial regulation of intestinal motility provides resistance against helminth infection
title_full Microbial regulation of intestinal motility provides resistance against helminth infection
title_fullStr Microbial regulation of intestinal motility provides resistance against helminth infection
title_full_unstemmed Microbial regulation of intestinal motility provides resistance against helminth infection
title_short Microbial regulation of intestinal motility provides resistance against helminth infection
title_sort microbial regulation of intestinal motility provides resistance against helminth infection
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9705251/
https://www.ncbi.nlm.nih.gov/pubmed/35288644
http://dx.doi.org/10.1038/s41385-022-00498-8
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