Abstract
BackgroundDynamic interactions between the host and gastrointestinal microbiota play an important role for local and systemic immune homeostasis. Helminthic parasites modulate the host immune response, resulting in protection against autoimmune disease but also increased susceptibility to pathogen infection. The underlying mechanisms remain largely unknown.ResultsWe showed that the type 2 immune response to enteric Nippostrongylus brasiliensis infection in mice was associated with altered intestinal mucin and AMP expression and shifts in microbiota composition. Most strikingly, infection reduced concentrations of intestinal segmented filamentous bacteria (SFB), known inducers of T helper 17 cells, and IL-17-associated gene expression. Infected mice deficient in IL-13 or STAT6 did not reduce SFB or IL-17, and exogenous IL-25 replicated the effects of parasite infection in wild type mice.ConclusionsOur data show that parasite infection acts through host type 2 immunity to reduce intestinal SFB and expression of IL-17, providing an example of a microbiota-dependent immune modulation by parasites.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0103-8) contains supplementary material, which is available to authorized users.
Highlights
Dynamic interactions between the host and gastrointestinal microbiota play an important role for local and systemic immune homeostasis
The infection up-regulated the expression of resistin-like molecule beta (Retnlb), angiogenin 4 (Ang4), and mucin 2 (Muc2) but down-regulated regenerating islet-derived protein 3 gamma (Reg3γ) and lysozymes 1 (Lyz1) and 2 (Lyz2) (Fig. 1c)
We found the expression of Muc2 and several antimicrobial peptides (AMP) with broad antimicrobial activity to be altered in response to N. brasiliensis infection, including Ang4, Reg3γ, and Lyz1 and Lyz2 [30]
Summary
Dynamic interactions between the host and gastrointestinal microbiota play an important role for local and systemic immune homeostasis. Helminthic parasites modulate the host immune response, resulting in protection against autoimmune disease and increased susceptibility to pathogen infection. Results: We showed that the type 2 immune response to enteric Nippostrongylus brasiliensis infection in mice was associated with altered intestinal mucin and AMP expression and shifts in microbiota composition. Infection reduced concentrations of intestinal segmented filamentous bacteria (SFB), known inducers of T helper 17 cells, and IL-17-associated gene expression. Homeostasis of the mammalian gastrointestinal (GI) tract depends on a complex network of interactions between the host and microbiota, including parasitic nematodes, bacteria, viruses, and others [1]. There has been growing interest in understanding the multilayered crosstalk and interactions between nematodes, commensal bacteria, and the host immune system given differences in disease expression in human populations where enteric helminth parasite infection is controlled compared to where it persists [11]. The cellular and molecular mechanisms underlying the potent immune modulating activities of nematodes remain elusive
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