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

Mario M. Zaiss, Alexis Rapin, Luc Lebon, Lalit Kumar Dubey, Ilaria Mosconi, Kerstin Sarter, Alessandra Piersigilli, Laure Menin, Alan W. Walker, Jacques Rougemont, Oonagh Paerewijck, Peter Geldhof, Kathleen D. McCoy, Andrew J. Macpherson, John Croese, Paul R. Giacomin, Alex Loukas, Tobias Junt, Benjamin J. Marsland, Nicola L. Harris

Research output: Contribution to journalArticleResearchpeer-review

Abstract

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.

Original languageEnglish
Pages (from-to)998-1010
Number of pages13
JournalImmunity
Volume43
Issue number5
DOIs
Publication statusPublished - 1 Jan 2015

Cite this

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. In: Immunity. 2015 ; Vol. 43, No. 5. pp. 998-1010.
@article{1837e808d5b34776b952e023794eced9,
title = "The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation",
abstract = "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.",
author = "Zaiss, {Mario M.} and Alexis Rapin and Luc Lebon and Dubey, {Lalit Kumar} and Ilaria Mosconi and Kerstin Sarter and Alessandra Piersigilli and Laure Menin and Walker, {Alan W.} and Jacques Rougemont and Oonagh Paerewijck and Peter Geldhof and McCoy, {Kathleen D.} and Macpherson, {Andrew J.} and John Croese and Giacomin, {Paul R.} and Alex Loukas and Tobias Junt and Marsland, {Benjamin J.} and Harris, {Nicola L.}",
year = "2015",
month = "1",
day = "1",
doi = "10.1016/j.immuni.2015.09.012",
language = "English",
volume = "43",
pages = "998--1010",
journal = "Immunity",
issn = "1074-7613",
publisher = "Elsevier",
number = "5",

}

Zaiss, MM, Rapin, A, Lebon, L, Dubey, LK, Mosconi, I, Sarter, K, Piersigilli, A, Menin, L, Walker, AW, Rougemont, J, Paerewijck, O, Geldhof, P, McCoy, KD, Macpherson, AJ, Croese, J, Giacomin, PR, Loukas, A, Junt, T, Marsland, BJ & Harris, NL 2015, 'The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation' Immunity, vol. 43, no. 5, pp. 998-1010. https://doi.org/10.1016/j.immuni.2015.09.012

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.

In: Immunity, Vol. 43, No. 5, 01.01.2015, p. 998-1010.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation

AU - Zaiss, Mario M.

AU - Rapin, Alexis

AU - Lebon, Luc

AU - Dubey, Lalit Kumar

AU - Mosconi, Ilaria

AU - Sarter, Kerstin

AU - Piersigilli, Alessandra

AU - Menin, Laure

AU - Walker, Alan W.

AU - Rougemont, Jacques

AU - Paerewijck, Oonagh

AU - Geldhof, Peter

AU - McCoy, Kathleen D.

AU - Macpherson, Andrew J.

AU - Croese, John

AU - Giacomin, Paul R.

AU - Loukas, Alex

AU - Junt, Tobias

AU - Marsland, Benjamin J.

AU - Harris, Nicola L.

PY - 2015/1/1

Y1 - 2015/1/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84947432484&partnerID=8YFLogxK

U2 - 10.1016/j.immuni.2015.09.012

DO - 10.1016/j.immuni.2015.09.012

M3 - Article

VL - 43

SP - 998

EP - 1010

JO - Immunity

JF - Immunity

SN - 1074-7613

IS - 5

ER -