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

doi:10.1016/j.immuni.2015.09.012

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 (Corresponding Author)

The Rowett Institute of Nutrition and Health

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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 language	English
Pages (from-to)	998-1010
Number of pages	13
Journal	Immunity
Volume	43
Issue number	5
Early online date	27 Oct 2015
DOIs	https://doi.org/10.1016/j.immuni.2015.09.012
Publication status	Published - 17 Nov 2015

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Immunity
This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial-No Derivs (CC BY-NC-ND 4.0) license, which permits others to distribute this work non-commercially provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc-nd/4.0/
Final published version, 4.14 MBLicence: CC BY-NC-ND

Alan Walker
- School of Medicine, Medical Sciences & Nutrition, The Rowett Institute of Nutrition and Health - Senior Lecturer
Person: Academic

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Zaiss, M. M., Rapin, A., Lebon, L., Dubey, L. K., Mosconi, I., Sarter, K., Piersigilli, A., Menin, L., Walker, A. W., Rougemont, J., Paerewijck, O., Geldhof, P., McCoy, K. D., Macpherson, A. J., Croese, J., Giacomin, P. R., Loukas, A., Junt, T., Marsland, B. J., & Harris, N. L. (2015). The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation. Immunity, 43(5), 998-1010. https://doi.org/10.1016/j.immuni.2015.09.012

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

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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}",

note = "We thank Manuel Kulagin for technical help, Pierre Bonnaventure for portal vein blood sampling, Francisco Sepulveda for technical assistance in GS-MS acquisition, and Dorothee Hahne (Metabolomics Australia, University of Western Australia) for human samples SCFA isolation, acquisition, and analysis. We also thank Cristina Cartoni (Phenotyping Unit, EPFL) for Milliplex analysis, Jessica Dessimoz and her team from the Histology Core Facility (EPFL), Miguel Garcia and his team from the Flow Cytometry Core Facility (EPFL), and staff from the EPFL CPG animal house for excellent animal care. The computations were partially performed at the Vital-IT Center for high-performance computing of the SIB Swiss Institute of Bioinformatics (http://www.vital-it.ch). The research leading to these results has received funding from the European Research Council under the European Union{\textquoteright}s Seventh Framework Programme (FP/2007-2013) / ERC Grant Agreement n. 310948. Funding for A.W.W. and a subset of the 16S rRNA gene sequencing was provided by the Wellcome Trust (grant number WT 098051). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. ",

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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

N1 - We thank Manuel Kulagin for technical help, Pierre Bonnaventure for portal vein blood sampling, Francisco Sepulveda for technical assistance in GS-MS acquisition, and Dorothee Hahne (Metabolomics Australia, University of Western Australia) for human samples SCFA isolation, acquisition, and analysis. We also thank Cristina Cartoni (Phenotyping Unit, EPFL) for Milliplex analysis, Jessica Dessimoz and her team from the Histology Core Facility (EPFL), Miguel Garcia and his team from the Flow Cytometry Core Facility (EPFL), and staff from the EPFL CPG animal house for excellent animal care. The computations were partially performed at the Vital-IT Center for high-performance computing of the SIB Swiss Institute of Bioinformatics (http://www.vital-it.ch). The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013) / ERC Grant Agreement n. 310948. Funding for A.W.W. and a subset of the 16S rRNA gene sequencing was provided by the Wellcome Trust (grant number WT 098051). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PY - 2015/11/17

Y1 - 2015/11/17

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.

U2 - 10.1016/j.immuni.2015.09.012

DO - 10.1016/j.immuni.2015.09.012

M3 - Article

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VL - 43

SP - 998

EP - 1010

JO - Immunity

JF - Immunity

SN - 1074-7613

IS - 5

ER -

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

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