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)

Research output: Contribution to journal › Article

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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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Final published version, 4.14 MBLicence: CC BY-NC-ND

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Alan Walker

School of Medicine, Medical Sciences & Nutrition, The Rowett Institute of Nutrition and Health - Senior Lecturer
Clinical Medicine

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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

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 (Corresponding Author).

In: Immunity, Vol. 43, No. 5, 17.11.2015, p. 998-1010.

Research output: Contribution to journal › Article

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

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.

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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.",

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AU - Sarter, Kerstin

AU - Piersigilli, Alessandra

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AU - Loukas, Alex

AU - Junt, Tobias

AU - Marsland, Benjamin J

AU - Harris, Nicola L

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