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)

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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 languageEnglish
Pages (from-to)998-1010
Number of pages13
JournalImmunity
Volume43
Issue number5
Early online date27 Oct 2015
DOIs
Publication statusPublished - 17 Nov 2015

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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