The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.

The digestive tract is the first organ affected by the ingestion of foodborne bacteria. While commensal bacteria become resident, opportunistic or virulent bacteria are eliminated from the gut by the local innate immune system. Here we characterize a new mechanism of defense, independent of the immu...

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Main Authors: Olivia Benguettat, Rouba Jneid, Julie Soltys, Rihab Loudhaief, Alexandra Brun-Barale, Dani Osman, Armel Gallet
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-09-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC6138423?pdf=render
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spelling doaj-154cda8f811f491fa900b34507d8318a2020-11-25T00:55:39ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742018-09-01149e100727910.1371/journal.ppat.1007279The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.Olivia BenguettatRouba JneidJulie SoltysRihab LoudhaiefAlexandra Brun-BaraleDani OsmanArmel GalletThe digestive tract is the first organ affected by the ingestion of foodborne bacteria. While commensal bacteria become resident, opportunistic or virulent bacteria are eliminated from the gut by the local innate immune system. Here we characterize a new mechanism of defense, independent of the immune system, in Drosophila melanogaster. We observed strong contractions of longitudinal visceral muscle fibers for the first 2 hours following bacterial ingestion. We showed that these visceral muscle contractions are induced by immune reactive oxygen species (ROS) that accumulate in the lumen and depend on the ROS-sensing TRPA1 receptor. We then demonstrate that both ROS and TRPA1 are required in a subset of anterior enteroendocrine cells for the release of the DH31 neuropeptide which activates its receptor in the neighboring visceral muscles. The resulting contractions of the visceral muscles favors quick expulsion of the bacteria, limiting their presence in the gut. Our results unveil a precocious mechanism of defense against ingested opportunistic bacteria, whether they are Gram-positive like Bacillus thuringiensis or Gram-negative like Erwinia carotovora carotovora. Finally, we found that the human homolog of DH31, CGRP, has a conserved function in Drosophila.http://europepmc.org/articles/PMC6138423?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Olivia Benguettat
Rouba Jneid
Julie Soltys
Rihab Loudhaief
Alexandra Brun-Barale
Dani Osman
Armel Gallet
spellingShingle Olivia Benguettat
Rouba Jneid
Julie Soltys
Rihab Loudhaief
Alexandra Brun-Barale
Dani Osman
Armel Gallet
The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
PLoS Pathogens
author_facet Olivia Benguettat
Rouba Jneid
Julie Soltys
Rihab Loudhaief
Alexandra Brun-Barale
Dani Osman
Armel Gallet
author_sort Olivia Benguettat
title The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
title_short The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
title_full The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
title_fullStr The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
title_full_unstemmed The DH31/CGRP enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
title_sort dh31/cgrp enteroendocrine peptide triggers intestinal contractions favoring the elimination of opportunistic bacteria.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2018-09-01
description The digestive tract is the first organ affected by the ingestion of foodborne bacteria. While commensal bacteria become resident, opportunistic or virulent bacteria are eliminated from the gut by the local innate immune system. Here we characterize a new mechanism of defense, independent of the immune system, in Drosophila melanogaster. We observed strong contractions of longitudinal visceral muscle fibers for the first 2 hours following bacterial ingestion. We showed that these visceral muscle contractions are induced by immune reactive oxygen species (ROS) that accumulate in the lumen and depend on the ROS-sensing TRPA1 receptor. We then demonstrate that both ROS and TRPA1 are required in a subset of anterior enteroendocrine cells for the release of the DH31 neuropeptide which activates its receptor in the neighboring visceral muscles. The resulting contractions of the visceral muscles favors quick expulsion of the bacteria, limiting their presence in the gut. Our results unveil a precocious mechanism of defense against ingested opportunistic bacteria, whether they are Gram-positive like Bacillus thuringiensis or Gram-negative like Erwinia carotovora carotovora. Finally, we found that the human homolog of DH31, CGRP, has a conserved function in Drosophila.
url http://europepmc.org/articles/PMC6138423?pdf=render
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