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Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling

Intestinal microbes impact the health of the intestine and organs distal to the gut. Limosilactobacillus reuteri is a human intestinal microbe that promotes normal gut transit, the anti-inflammatory immune system, wound healing, normal social behavior in mice, and prevents bone reabsorption. Oxytoci...

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Autores principales: Danhof, Heather A., Lee, Jihwan, Thapa, Aanchal, Britton, Robert A., Di Rienzi, Sara C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10498800/
https://www.ncbi.nlm.nih.gov/pubmed/37698879
http://dx.doi.org/10.1080/19490976.2023.2256043
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author Danhof, Heather A.
Lee, Jihwan
Thapa, Aanchal
Britton, Robert A.
Di Rienzi, Sara C.
author_facet Danhof, Heather A.
Lee, Jihwan
Thapa, Aanchal
Britton, Robert A.
Di Rienzi, Sara C.
author_sort Danhof, Heather A.
collection PubMed
description Intestinal microbes impact the health of the intestine and organs distal to the gut. Limosilactobacillus reuteri is a human intestinal microbe that promotes normal gut transit, the anti-inflammatory immune system, wound healing, normal social behavior in mice, and prevents bone reabsorption. Oxytocin impacts these functions and oxytocin signaling is required for L. reuteri-mediated wound healing and social behavior; however, the events in the gut leading to oxytocin stimulation and beneficial effects are unknown. Here we report evolutionarily conserved oxytocin production in the intestinal epithelium through analysis of single-cell RNA-Seq datasets and imaging of human and mouse intestinal tissues. Moreover, human intestinal organoids produce oxytocin, demonstrating that the intestinal epithelium is sufficient to produce oxytocin. We find that L. reuteri facilitates oxytocin secretion from human intestinal tissue and human intestinal organoids. Finally, we demonstrate that stimulation of oxytocin secretion by L. reuteri is dependent on the gut hormone secretin, which is produced in enteroendocrine cells, while oxytocin itself is produced in enterocytes. Altogether, this work demonstrates that oxytocin is produced and secreted from enterocytes in the intestinal epithelium in response to secretin stimulated by L. reuteri. This work thereby identifies oxytocin as an intestinal hormone and provides mechanistic insight into avenues by which gut microbes promote host health.
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spelling pubmed-104988002023-09-14 Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling Danhof, Heather A. Lee, Jihwan Thapa, Aanchal Britton, Robert A. Di Rienzi, Sara C. Gut Microbes Research Paper Intestinal microbes impact the health of the intestine and organs distal to the gut. Limosilactobacillus reuteri is a human intestinal microbe that promotes normal gut transit, the anti-inflammatory immune system, wound healing, normal social behavior in mice, and prevents bone reabsorption. Oxytocin impacts these functions and oxytocin signaling is required for L. reuteri-mediated wound healing and social behavior; however, the events in the gut leading to oxytocin stimulation and beneficial effects are unknown. Here we report evolutionarily conserved oxytocin production in the intestinal epithelium through analysis of single-cell RNA-Seq datasets and imaging of human and mouse intestinal tissues. Moreover, human intestinal organoids produce oxytocin, demonstrating that the intestinal epithelium is sufficient to produce oxytocin. We find that L. reuteri facilitates oxytocin secretion from human intestinal tissue and human intestinal organoids. Finally, we demonstrate that stimulation of oxytocin secretion by L. reuteri is dependent on the gut hormone secretin, which is produced in enteroendocrine cells, while oxytocin itself is produced in enterocytes. Altogether, this work demonstrates that oxytocin is produced and secreted from enterocytes in the intestinal epithelium in response to secretin stimulated by L. reuteri. This work thereby identifies oxytocin as an intestinal hormone and provides mechanistic insight into avenues by which gut microbes promote host health. Taylor & Francis 2023-09-12 /pmc/articles/PMC10498800/ /pubmed/37698879 http://dx.doi.org/10.1080/19490976.2023.2256043 Text en © 2023 The Author(s). Published with license by Taylor & Francis Group, LLC. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.
spellingShingle Research Paper
Danhof, Heather A.
Lee, Jihwan
Thapa, Aanchal
Britton, Robert A.
Di Rienzi, Sara C.
Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title_full Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title_fullStr Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title_full_unstemmed Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title_short Microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
title_sort microbial stimulation of oxytocin release from the intestinal epithelium via secretin signaling
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10498800/
https://www.ncbi.nlm.nih.gov/pubmed/37698879
http://dx.doi.org/10.1080/19490976.2023.2256043
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