Abstract
Diet composition may play a crucial role in shaping host immune responses and commensal gut microbiota populations. Bioactive dietary components, such as inulin, have been extensively studied for their bioactive properties, particularly in modulating gut immune function and reducing inflammation. It has been shown that colonization with gastrointestinal parasitic worms (helminths) may alleviate chronic inflammation through promotion of T-helper cell type (Th) 2 and T-regulatory immune responses and alterations in the gut microbiome. In this study, we investigated if dietary inulin could modulate mucosal immune function in pigs during colonization with the porcine whipworm Trichuris suis. T. suis infection induced a typical Th2-biased immune response characterized by transcriptional changes in Th2- and barrier function-related genes, accompanied by intestinal remodeling through increased epithelial goblet and tuft cell proliferation. We observed that inulin also up-regulated Th2-related immune genes (IL13, IL5), and suppressed Th1-related pro-inflammatory genes (IFNG, IL1A, IL8) in the colon. Notably, inulin augmented the T. suis-induced responses with increased transcription of key Th2 and mucosal barrier genes (e.g., IL13, TFF3), and synergistically suppressed pro-inflammatory genes, such as IFNG and CXCL9. 16S rRNA sequencing of proximal colon digesta samples revealed that inulin supplementation reduced the abundance of bacterial phyla linked to inflammation, such as Proteobacteria and Firmicutes, and simultaneously increased Actinobacteria and Bacteroidetes. Interestingly, pigs treated with both inulin and T. suis displayed the highest Bacteroidetes: Firmicutes ratio and the lowest gut pH, suggesting an interaction of diet and helminth infection that stimulates the growth of beneficial bacterial species. Overall, our data demonstrate that T. suis infection and inulin co-operatively enhance anti-inflammatory immune responses, which is potentially mediated by changes in microbiota composition. Our results highlight the intricate interactions between diet, immune function and microbiota composition in a porcine helminth infection model. This porcine model should facilitate further investigations into the use of bioactive diets as immunomodulatory mediators against inflammatory conditions, and how diet and parasites may influence gut health.
Highlights
Gut health and mucosal immune function may be considerably influenced by diet, and there is increasing interest in the role of bioactive dietary components as functional food ingredients that may modulate chronic inflammation and immune responses to gastrointestinal microbes
Of infection, the leukocyte profile in peripheral blood mononuclear cells (PBMCs) showed that dietary inulin significantly decreased the proportion of CD3+ T cells at day 14 (p < 0.05) and day 28 p.i. (p < 0.005, Figures 1A,B)
Interactions between diet and the gut microbiota likely have a pronounced effect on mucosal immune function, and so we investigated in detail how dietary inulin and/or T. suis infection modified the transcription of immune, inflammation and mucosal barrier-related genes in the proximal colon
Summary
Gut health and mucosal immune function may be considerably influenced by diet, and there is increasing interest in the role of bioactive dietary components as functional food ingredients that may modulate chronic inflammation and immune responses to gastrointestinal microbes. The functional activity of these mucosal immune cells can be regulated by a variety of different commensal microbes and their products, or external stimuli, such as dietary compounds and gastrointestinal pathogens. Dietary-mediated immunomodulation can occur (i) indirectly through prebiotic modification of the commensal gut microbiota, whereby microbial-derived products, such as short-chain fatty acids (SCFAs) can induce tolerogenic activity in dendritic cells (DCs) and T-cells [2, 3], as well as enhance mucus production and barrier function [4, 5], or (ii) by direct interaction of dietary compounds with the epithelial cell barrier and intestinal immune cells [6]. Bioactive dietary components with either prebiotic or direct stimulatory effects may play a major role in modulating mucosal immune function
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