Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis

Aurélien Trompette, Eva S. Gollwitzer, Koshika Yadava, Anke K. Sichelstiel, Norbert Sprenger, Catherine Ngom-Bru, Carine Blanchard, Tobias Junt, Laurent P. Nicod, Nicola L. Harris, Benjamin J. Marsland

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Metabolites from intestinal microbiota are key determinants of host-microbe mutualism and, consequently, the health or disease of the intestinal tract. However, whether such host-microbe crosstalk influences inflammation in peripheral tissues, such as the lung, is poorly understood. We found that dietary fermentable fiber content changed the composition of the gut and lung microbiota, in particular by altering the ratio of Firmicutes to Bacteroidetes. The gut microbiota metabolized the fiber, consequently increasing the concentration of circulating short-chain fatty acids (SCFAs). Mice fed a high-fiber diet had increased circulating levels of SCFAs and were protected against allergic inflammation in the lung, whereas a low-fiber diet decreased levels of SCFAs and increased allergic airway disease. Treatment of mice with the SCFA propionate led to alterations in bone marrow hematopoiesis that were characterized by enhanced generation of macrophage and dendritic cell (DC) precursors and subsequent seeding of the lungs by DCs with high phagocytic capacity but an impaired ability to promote T helper type 2 (T H 2) cell effector function. The effects of propionate on allergic inflammation were dependent on G protein-coupled receptor 41 (GPR41, also called free fatty acid receptor 3 or FFAR3), but not GPR43 (also called free fatty acid receptor 2 or FFAR2). Our results show that dietary fermentable fiber and SCFAs can shape the immunological environment in the lung and influence the severity of allergic inflammation.

Original languageEnglish
Pages (from-to)159-166
Number of pages8
JournalNature Medicine
Volume20
Issue number2
DOIs
Publication statusPublished - 1 Feb 2014

Cite this

Trompette, A., Gollwitzer, E. S., Yadava, K., Sichelstiel, A. K., Sprenger, N., Ngom-Bru, C., ... Marsland, B. J. (2014). Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nature Medicine, 20(2), 159-166. https://doi.org/10.1038/nm.3444
Trompette, Aurélien ; Gollwitzer, Eva S. ; Yadava, Koshika ; Sichelstiel, Anke K. ; Sprenger, Norbert ; Ngom-Bru, Catherine ; Blanchard, Carine ; Junt, Tobias ; Nicod, Laurent P. ; Harris, Nicola L. ; Marsland, Benjamin J. / Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. In: Nature Medicine. 2014 ; Vol. 20, No. 2. pp. 159-166.
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Trompette, A, Gollwitzer, ES, Yadava, K, Sichelstiel, AK, Sprenger, N, Ngom-Bru, C, Blanchard, C, Junt, T, Nicod, LP, Harris, NL & Marsland, BJ 2014, 'Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis' Nature Medicine, vol. 20, no. 2, pp. 159-166. https://doi.org/10.1038/nm.3444

Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. / Trompette, Aurélien; Gollwitzer, Eva S.; Yadava, Koshika; Sichelstiel, Anke K.; Sprenger, Norbert; Ngom-Bru, Catherine; Blanchard, Carine; Junt, Tobias; Nicod, Laurent P.; Harris, Nicola L.; Marsland, Benjamin J.

In: Nature Medicine, Vol. 20, No. 2, 01.02.2014, p. 159-166.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Sprenger, Norbert

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Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nature Medicine. 2014 Feb 1;20(2):159-166. https://doi.org/10.1038/nm.3444