Cargando…

The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation

Intestinal helminths are potent regulators of their host’s immune system and can ameliorate inflammatory diseases such as allergic asthma. In the present study we have assessed whether this anti-inflammatory activity was purely intrinsic to helminths, or whether it also involved crosstalk with the l...

Descripción completa

Detalles Bibliográficos
Autores principales: Zaiss, Mario M., Rapin, Alexis, Lebon, Luc, Dubey, Lalit Kumar, Mosconi, Ilaria, Sarter, Kerstin, Piersigilli, Alessandra, Menin, Laure, Walker, Alan W., Rougemont, Jacques, Paerewijck, Oonagh, Geldhof, Peter, McCoy, Kathleen D., Macpherson, Andrew J., Croese, John, Giacomin, Paul R., Loukas, Alex, Junt, Tobias, Marsland, Benjamin J., Harris, Nicola L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4658337/
https://www.ncbi.nlm.nih.gov/pubmed/26522986
http://dx.doi.org/10.1016/j.immuni.2015.09.012
_version_ 1782402502298173440
author Zaiss, Mario M.
Rapin, Alexis
Lebon, Luc
Dubey, Lalit Kumar
Mosconi, Ilaria
Sarter, Kerstin
Piersigilli, Alessandra
Menin, Laure
Walker, Alan W.
Rougemont, Jacques
Paerewijck, Oonagh
Geldhof, Peter
McCoy, Kathleen D.
Macpherson, Andrew J.
Croese, John
Giacomin, Paul R.
Loukas, Alex
Junt, Tobias
Marsland, Benjamin J.
Harris, Nicola L.
author_facet Zaiss, Mario M.
Rapin, Alexis
Lebon, Luc
Dubey, Lalit Kumar
Mosconi, Ilaria
Sarter, Kerstin
Piersigilli, Alessandra
Menin, Laure
Walker, Alan W.
Rougemont, Jacques
Paerewijck, Oonagh
Geldhof, Peter
McCoy, Kathleen D.
Macpherson, Andrew J.
Croese, John
Giacomin, Paul R.
Loukas, Alex
Junt, Tobias
Marsland, Benjamin J.
Harris, Nicola L.
author_sort Zaiss, Mario M.
collection PubMed
description Intestinal helminths are potent regulators of their host’s immune system and can ameliorate inflammatory diseases such as allergic asthma. In the present study we have assessed whether this anti-inflammatory activity was purely intrinsic to helminths, or whether it also involved crosstalk with the local microbiota. We report that chronic infection with the murine helminth Heligmosomoides polygyrus bakeri (Hpb) altered the intestinal habitat, allowing increased short chain fatty acid (SCFA) production. Transfer of the Hpb-modified microbiota alone was sufficient to mediate protection against allergic asthma. The helminth-induced anti-inflammatory cytokine secretion and regulatory T cell suppressor activity that mediated the protection required the G protein-coupled receptor (GPR)-41. A similar alteration in the metabolic potential of intestinal bacterial communities was observed with diverse parasitic and host species, suggesting that this represents an evolutionary conserved mechanism of host-microbe-helminth interactions.
format Online
Article
Text
id pubmed-4658337
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Cell Press
record_format MEDLINE/PubMed
spelling pubmed-46583372016-01-11 The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation Zaiss, Mario M. Rapin, Alexis Lebon, Luc Dubey, Lalit Kumar Mosconi, Ilaria Sarter, Kerstin Piersigilli, Alessandra Menin, Laure Walker, Alan W. Rougemont, Jacques Paerewijck, Oonagh Geldhof, Peter McCoy, Kathleen D. Macpherson, Andrew J. Croese, John Giacomin, Paul R. Loukas, Alex Junt, Tobias Marsland, Benjamin J. Harris, Nicola L. Immunity Article Intestinal helminths are potent regulators of their host’s immune system and can ameliorate inflammatory diseases such as allergic asthma. In the present study we have assessed whether this anti-inflammatory activity was purely intrinsic to helminths, or whether it also involved crosstalk with the local microbiota. We report that chronic infection with the murine helminth Heligmosomoides polygyrus bakeri (Hpb) altered the intestinal habitat, allowing increased short chain fatty acid (SCFA) production. Transfer of the Hpb-modified microbiota alone was sufficient to mediate protection against allergic asthma. The helminth-induced anti-inflammatory cytokine secretion and regulatory T cell suppressor activity that mediated the protection required the G protein-coupled receptor (GPR)-41. A similar alteration in the metabolic potential of intestinal bacterial communities was observed with diverse parasitic and host species, suggesting that this represents an evolutionary conserved mechanism of host-microbe-helminth interactions. Cell Press 2015-11-17 /pmc/articles/PMC4658337/ /pubmed/26522986 http://dx.doi.org/10.1016/j.immuni.2015.09.012 Text en © 2015 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Zaiss, Mario M.
Rapin, Alexis
Lebon, Luc
Dubey, Lalit Kumar
Mosconi, Ilaria
Sarter, Kerstin
Piersigilli, Alessandra
Menin, Laure
Walker, Alan W.
Rougemont, Jacques
Paerewijck, Oonagh
Geldhof, Peter
McCoy, Kathleen D.
Macpherson, Andrew J.
Croese, John
Giacomin, Paul R.
Loukas, Alex
Junt, Tobias
Marsland, Benjamin J.
Harris, Nicola L.
The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title_full The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title_fullStr The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title_full_unstemmed The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title_short The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation
title_sort intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4658337/
https://www.ncbi.nlm.nih.gov/pubmed/26522986
http://dx.doi.org/10.1016/j.immuni.2015.09.012
work_keys_str_mv AT zaissmariom theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT rapinalexis theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT lebonluc theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT dubeylalitkumar theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT mosconiilaria theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT sarterkerstin theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT piersigillialessandra theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT meninlaure theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT walkeralanw theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT rougemontjacques theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT paerewijckoonagh theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT geldhofpeter theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT mccoykathleend theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT macphersonandrewj theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT croesejohn theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT giacominpaulr theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT loukasalex theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT junttobias theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT marslandbenjaminj theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT harrisnicolal theintestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT zaissmariom intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT rapinalexis intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT lebonluc intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT dubeylalitkumar intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT mosconiilaria intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT sarterkerstin intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT piersigillialessandra intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT meninlaure intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT walkeralanw intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT rougemontjacques intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT paerewijckoonagh intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT geldhofpeter intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT mccoykathleend intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT macphersonandrewj intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT croesejohn intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT giacominpaulr intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT loukasalex intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT junttobias intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT marslandbenjaminj intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation
AT harrisnicolal intestinalmicrobiotacontributestotheabilityofhelminthstomodulateallergicinflammation