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Review
. 2018 Jan 24:9:5.
doi: 10.3389/fimmu.2018.00005. eCollection 2018.

Nutrients Mediate Intestinal Bacteria-Mucosal Immune Crosstalk

Ning Ma  1 , Pingting Guo  1 , Jie Zhang  1   2 , Ting He  1 , Sung Woo Kim  3 , Guolong Zhang  4 , Xi Ma  1   5   6
Affiliations
Review

Nutrients Mediate Intestinal Bacteria-Mucosal Immune Crosstalk

Ning Ma et al. Front Immunol. .

Abstract

The intestine is the shared site of nutrient digestion, microbiota colonization and immune cell location and this geographic proximity contributes to a large extent to their interaction. The onset and development of a great many diseases, such as inflammatory bowel disease and metabolic syndrome, will be caused due to the imbalance of body immune. As competent assistants, the intestinal bacteria are also critical in disease prevention and control. Moreover, the gut commensal bacteria are essential for development and normal operation of immune system and the pathogens are also closely bound up with physiological disorders and diseases mediated by immune imbalance. Understanding how our diet and nutrient affect bacterial composition and dynamic function, and the innate and adaptive status of our immune system, represents not only a research need but also an opportunity or challenge to improve health. Herein, this review focuses on the recent discoveries about intestinal bacteria-immune crosstalk and nutritional regulation on their interplay, with an aim to provide novel insights that can aid in understanding their interactions.

Keywords: bacteria; crosstalk; intestine; mucosal immunity; nutrients.

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Figures

Figure 1
Figure 1
Effects of gut microbes on innate immune receptor. (A) Bifidobacterium infantis 35624 treatment increases IL-10 secretion through the TLR2/TLR6 pathway in human myloid dendritic cell (mDC) and monocyte-derived DC (MDDC), while IL-10 secretion in plasmacytoid DC (pDC) is TLR9 dependent. (B) Lactobacillus acidophilus NCFM facilitates murine myeloid DC to express antiviral genes, such as myxovirus resistance 1, interferon (IFN)-β and interferon-stimulated gene 56 (Isg56), via TLR2 pathway. (C) Lactobacillus delbrueckii subsp. delbrueckii TUA4408L (Ld) response against Enterotoxigenic Escherichia coli (ETEC) 987P infection in porcine intestinal epithelial cells. Acidic extracellular polysaccharide (APS) and neutral extracellular polysaccharide (NPS) of Ld attenuate inflammation dependent on TLR2 and TLR4, respectively. (D) Non-invasive Helicobacter pylori infection in NOD2−/− mice relies on NOD2 signaling to induce Th1 inflammation response. (E) Non-invasive Clostridium difficile infection recruits neutrophils to infection sites via nucleotide-binding oligomerization domain protein 1 (NOD1). (F) Citrobacter rodentium induces inflammation exacerbation in NLRC4−/− mice by producing IL17A and IFN-γ.
Figure 2
Figure 2
The effects of gut bacteria on T cells differentiation. (A) The polysaccharide A of segmented filamentous bacteria (SFB) induces Th17 cells differentiation and the antigen of SFB presented by dendritic cell (DC) is dependent on major histocompatibility complex II (MHCII). SFB adhesion induces Th17 accumulation by producing serum amyloid A (SAA) and reactive oxygen species (ROS). (B) The Bacteroides fragilis improves Treg cells differentiation mediated by PSA-activated DC. (C) Clostridia species induces Tregs accumulation presumably by cooperating with DC in the colon. (D) Butyrate, a large intestinal bacterial metabolite, drives colonic expansion of Treg cells in mice by reinforcing histone H3 acetylation in the promoter and conserving non-coding sequence regions of the Foxp3 locus. (E) Bacteria-producing Zwitterionic capsular polysaccharides (ZPS) can stimulate differentiation of Treg cells and IL-10 production dependent on antigen-presenting cell (APC). (F) Commensal A4 bacteria of Lachnospiraceae family inhibit Th2 cells production by increasing transforming growth factor-β (TGF-β) production of DC. (G) The Th17 cells produce IL-17, IL-21, and IL-22 to enhance inflammation response, while the Treg cells produce IL-10 to attenuate inflammation.
Figure 3
Figure 3
The effect of nutrients at the interface of host immunity. (A) The absence of branched-chain amino acids (BCAA) impairs the innate immune function due to the shortage of lymphocytes and white blood cells. BCAA can also stimulate the secretion of SIgA to improve the mucosal surface defense and inhibit pathogen introgression into the lamina propria. (B) Trytophan (Trp) is absorbed by intestinal epithelial cells (IECs) directly activates the mTOR pathway by intracellular Trp receptors through a PI3K/AKT independent mechanism. The active mTOR connects metabolism and immunity, promoting cellular processes, and regulating AMPs expression. (C) Fructo-oligosaccharide and inulin are considered as prebiotics, affecting IECs to be hyporesponsive to activate nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) and mitogen-activated protein kinase (MAPK) induced by pathogens. Inflammatory response to lipopolysaccharide (LPS) would also be attenuated in this process. (D) G. lucidum polysaccharides (GLP) can effectively ameliorate the sensitivity of insulin, reducing low-grade chronic inflammation and inhibiting the outflux of plasma triglyceride and non-esterified fatty acid by suppressing the expression of tumor necrosis factor-a (TNF-α), interleukin-6 (IL-6), and hormone-sensitive lipase. (E) After ginseng polysaccharides (GS-P) treatment, the secretion of tumor necrosis factor-α (TNF-α) and interleukin-12 (IL-12) are increased and the macrophage and NK cell are activated. They both suppress the tumor metastasis.
Figure 4
Figure 4
Tryptophan mediates the bacteria–immune crosstalk. When induced by proinflammatory cytokines, the majority of tryptophan is metabolized through the kynurenine (Kyn) pathway mediated by indoleamine 2,3-dioxygenase (IDO). Kyn can serve as agonists for aryl hydrocarbon receptor (AhR), and act on dendritic cell (DCs) to inhibit DCs maturation. Through AhR, Kyn can cause T cell energy loss and apoptosis, promote the proliferation of Treg and Th17 cells, and also decrease the differentiation of highly inflammatory Th17 cells and enhance the generation of IL-22 and IL-10. Tryptophan can be degraded to 5-HT by the aid of Tryptophan hydroxylase gene (TPH1). Corynebacterium spp., Streptococcus spp., and Escherichia coli can also synthesize 5-HT themselves from tryptophan. Spore-forming bacteria (Sp) can regulate the concentration and synthesis of 5-HT. Melatonin can be then secreted after 5-HT, which can affect the differentiation of Th17 cells in the intestine.
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