Fructooligosaccharides protect against OVA-induced food allergy in mice by regulating the Th17/Treg cell balance using tryptophan metabolites

Yan, Xiumei; Yan, Jingbin; Xiang, Qiangwei; Wang, Fanyan; Dai, Huan; Huang, Kaiyu; Fang, Ling-Juan; Yao, Hao; Wang, Lingya; Zhang, Weixi

doi:10.1039/d0fo03371e

Cited by 30 publications

(26 citation statements)

References 65 publications

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“…Fucose increased the abundance of Trp-producing E. coli and normalized the blood Trp levels [ 45 ]. Fructooligosaccharides (FOS) modulated the gut microbiome profiles, such as an increase in the abundance of Ruminococcacere (phylum level) and a decrease in the abundance of Akkermansiaceae (family level) and Verrucomicrobia (phylum level), and significantly increased the levels of Trp and 5-hydroxytryptamine (5-HT) [ 46 ]. The ginseng polysaccharides decreased L-kynurenine, as well as the ratio of Kyn/Trp [ 47 ].…”

Section: Trp Metabolism In Gut Microbiotamentioning

confidence: 99%

Gut Microbiota-Derived Tryptophan Metabolites Maintain Gut and Systemic Homeostasis

Gao

Yang

2022

Cells

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Tryptophan is an essential amino acid from dietary proteins. It can be metabolized into different metabolites in both the gut microbiota and tissue cells. Tryptophan metabolites such as indole-3-lactate (ILA), indole-3-acrylate (IAC), indole-3-propionate (IPA), indole-3-aldehyde (IAID), indoleacetic acid (IAA), indole-3-acetaldehyde and Kyn can be produced by intestinal microorganisms through direct Trp transformation and also, partly, the kynurenine (Kyn) pathway. These metabolites play a critical role in maintaining the homeostasis of the gut and systematic immunity and also potentially affect the occurrence and development of diseases such as inflammatory bowel diseases, tumors, obesity and metabolic syndrome, diseases in the nervous system, infectious diseases, vascular inflammation and cardiovascular diseases and hepatic fibrosis. They can not only promote the differentiation and function of anti-inflammatory macrophages, Treg cells, CD4+CD8αα+ regulatory cells, IL-10+ and/or IL-35+B regulatory cells but also IL-22-producing innate lymphoid cells 3 (ILC3), which are involved in maintaining the gut mucosal homeostasis. These findings have important consequences in the immunotherapy against tumor and other immune-associated diseases. We will summarize here the recent advances in understanding the generation and regulation of tryptophan metabolites in the gut microbiota, the role of gut microbiota-derived tryptophan metabolites in different immune cells, the occurrence and development of diseases and immunotherapy against immune-associated diseases.

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Section: Trp Metabolism In Gut Microbiotamentioning

confidence: 99%

Gut Microbiota-Derived Tryptophan Metabolites Maintain Gut and Systemic Homeostasis

Gao

Yang

2022

Cells

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“…It has been reported that changes in the composition of the gut microbiota are associated with the development of FA [ 43 ]. Previous studies showed that the abundance of Firmicutes and Clostridia were reduced in patients with milk allergies, and the Firmicutes and Ruminococcaceae were lower in mice with OVA-induced FA [ 6 ]. This study revealed a significant decrease in the abundance of Firmicutes in OVA-sensitized mice, which was associated with an aggravated response to food antigens [ 5 ].…”

Section: Discussionmentioning

confidence: 99%

“…However, polyphenolic compounds, especially anthocyanins, are susceptible to structural decomposition in the gastrointestinal tract, severely limiting their biological activity [ 4 ]. Recent studies have emphasized that intestinal ecological imbalance, including intestinal immune homeostasis and bacterial structure imbalance, plays a vital role in the occurrence and development of FA [ 5 , 6 ]. Therefore, to improve the anti-FA bioactivity of dietary polyphenols, they must reach the lower gastrointestinal tract intact to fully regulate intestinal ecological balance.…”

Section: Introductionmentioning

confidence: 99%

“…For example, colonizing germ-free mice with Clostridial taxa reportedly protected against oral allergenic sensitization [ 19 ]. Moreover, beneficial intestinal bacteria can directly stimulate the intestinal immune system to express anti-inflammatory cytokines (e.g., interleukin (IL)-10) and regulate mucosal integrity by producing metabolites, such as short chain fatty acids (SCFAs) [ 6 , 18 ]. Therefore, taking into account the role of gut ecological balance in the regulation of FA and the advantages of polysaccharide-based encapsulation for targeted intestinal delivery of polyphenols mentioned above, it is reasonable to hypothesize that polyphenols retained in higher amounts in the intestine after polysaccharide encapsulation may exert better anti-allergic activity through better regulation of intestinal ecological balance.…”

Section: Introductionmentioning

confidence: 99%

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Amelioration of Ovalbumin-Induced Food Allergy in Mice by Targeted Rectal and Colonic Delivery of Cyanidin-3-O-Glucoside

Zou²,

Liu

2022

Foods

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Targeted rectal and colonic delivery is an effective strategy to exploit the biological functions of polyphenols. This work investigated the anti-food allergy (FA) activity of cyanidin-3-O-glucoside (C3G) delivered by enteric sodium alginate in vivo. The results showed that through targeted rectal and colonic delivery, the C3G showed better results in ameliorating clinical allergic symptoms, diarrhea, and serological indicators including ovalbumin-specific IgE, histamine, and mast cell protease-1. The C3G was more efficient in enhancing the intestinal epithelial barrier by up-regulating the tight junction protein expression and promoting secretory IgA and β-defensin secretion. The improved bioactivity in regulating T helper (Th)1/Th2 immune balance in the intestinal mucosa was also observed. Compared with the intestinal microbiota structure of the model group, targeted rectal and colonic delivery of C3G was able to bring the abundance of Bacteroidota and Firmicutes close to the levels found in normal mice. Furthermore, there was an evident increase in beneficial bacteria in the intestinal flora, such as Lactobacillus and Odoribacter, and a decrease in pathogenic bacteria like Helicobacter and Turicibacter. Therefore, the anti-FA activity of C3G could be increased via targeted rectal and colonic delivery, while the mechanism might be attributed to the regulation of intestinal microecological homeostasis.

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“…Changes in tryptophan metabolites significantly affect the clinical characteristics of patients with food allergies [ 17 ], depression [ 18 ], and cancer [ 19 ]. Fructooligosaccharides significantly increased kynurenine levels and restored Th17/Treg balance to alleviate the clinical manifestations in mice with ovalbumin-induced food allergies [ 20 ]. Fuzhuan brick tea polysaccharide increased indoleacetic acid (IAA) and indole-3-aldehyde (IAld) levels and thus activated the aryl hydrocarbon receptor (AHR) signaling pathway to improve ulcerative colitis via producing interleukin-22 (IL-22) and evaluating the expression of intestinal tight junction proteins [ 21 ].…”

Section: Introductionmentioning

confidence: 99%

Limosilactobacillus reuteri Attenuates Atopic Dermatitis via Changes in Gut Bacteria and Indole Derivatives from Tryptophan Metabolism

Fang

Pan

Wang

et al. 2022

IJMS

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Gut bacteria are closely associated with the development of atopic dermatitis (AD) due to their immunoregulatory function. Indole derivatives, produced by gut bacteria metabolizing tryptophan, are ligands to activate the aryl hydrocarbon receptor (AHR), which plays a critical role in attenuating AD symptoms. Limosilactobacillus reuteri, a producer of indole derivatives, regulates mucosal immunity via activating the AHR signaling pathway. However, the effective substance and mechanism of L. reuteri in the amelioration of AD remain to be elucidated. In this research, we found that L. reuteri DYNDL22M62 significantly improved AD-like symptoms in mice by suppressing IgE levels and the expressions of thymic stromal lymphopoietin (TSLP), IL-4, and IL-5. L. reuteri DYNDL22M62 induced an increase in the production of indole lactic acid (ILA) and indole propionic acid (IPA) via targeted tryptophan metabolic analysis and the expression of AHR in mice. Furthermore, L. reuteri DYNDL22M62 increased the proportions of Romboutsia and Ruminococcaceae NK4A214 group, which were positively related to ILA, but decreased Dubosiella, which was negatively related to IPA. Collectively, L. reuteri DYNDL22M62 with the role of modulating gut bacteria and the production of indole derivatives may attenuate AD via activating AHR in mice.

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Fructooligosaccharides protect against OVA-induced food allergy in mice by regulating the Th17/Treg cell balance using tryptophan metabolites

Abstract: Fructooligosaccharides (Fos) can change gut microbiota composition and play a protective role against food allergy (FA). Furthermore, the protective mechanism of Fos against FA is unclear. In this study, intestinal...

Cited by 30 publications

References 65 publications

Gut Microbiota-Derived Tryptophan Metabolites Maintain Gut and Systemic Homeostasis

Gut Microbiota-Derived Tryptophan Metabolites Maintain Gut and Systemic Homeostasis

Amelioration of Ovalbumin-Induced Food Allergy in Mice by Targeted Rectal and Colonic Delivery of Cyanidin-3-O-Glucoside

Limosilactobacillus reuteri Attenuates Atopic Dermatitis via Changes in Gut Bacteria and Indole Derivatives from Tryptophan Metabolism

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