Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα
Inflammatory bowel disease (IBD) is a chronic progressive intestinal inflammatory disease, characterized by an altered gut microbiota composition and accompanying alterations in circulatory bile acids. Increasing evidence supports the beneficial effect of probiotics intake on health. Introduction of...
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Frontiers Media S.A.
2022-04-01
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| Series: | Frontiers in Nutrition |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnut.2022.816836/full |
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| author | Wing-Yan Wong Wing-Yan Wong Brandon Dow Chan Brandon Dow Chan Tung-Ting Sham Magnolia Muk-Lan Lee Magnolia Muk-Lan Lee Chi-On Chan Chi-On Chan Chung-Ting Chau Daniel Kam-Wah Mok Daniel Kam-Wah Mok Daniel Kam-Wah Mok Yiu-Wa Kwan William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai |
| author_facet | Wing-Yan Wong Wing-Yan Wong Brandon Dow Chan Brandon Dow Chan Tung-Ting Sham Magnolia Muk-Lan Lee Magnolia Muk-Lan Lee Chi-On Chan Chi-On Chan Chung-Ting Chau Daniel Kam-Wah Mok Daniel Kam-Wah Mok Daniel Kam-Wah Mok Yiu-Wa Kwan William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai |
| author_sort | Wing-Yan Wong |
| collection | DOAJ |
| description | Inflammatory bowel disease (IBD) is a chronic progressive intestinal inflammatory disease, characterized by an altered gut microbiota composition and accompanying alterations in circulatory bile acids. Increasing evidence supports the beneficial effect of probiotics intake on health. Introduction of probiotics to the intestines can modulate gut microbiota composition and in turn regulate the host immune system and modify the inflammatory response. Probiotics can also improve intestinal barrier function and exhibit a positive impact on host physiological and pathological conditions via gut microbiota-derived metabolites. Previous studies have demonstrated that Lactobacillus casei strain Shirota (LcS) treatment could inhibit clinical manifestation of colitis in dextran sulfate sodium (DSS)-induced mice, however, the underlying mechanisms remain unknown. In this study, we employed the DSS-induced acute colitis mouse model to investigate the anti-inflammatory effects of LcS and related mechanisms. Administration of LcS ameliorated the severity of DSS-induced colitis and enhanced intestinal integrity via induction of mucin-2 and occludin expression in colons. Fecal microbiota analysis showed that LcS increased the relative abundance of beneficial bacterial species in colitic mice, whereas the relative abundance of pathobionts was reduced. Additionally, LcS treatment modulated circulating bile acid profiles in colitic mice. In mice treated with LcS, we identified increased levels of primary taurine-conjugated bile acids, including taurocholic acid (TCA) and taurochenodeoxycholic acid (TCDCA). LcS treatment also increased the levels of secondary taurine-conjugated bile acids, including taurodeoxycholic acid (TDCA) and tauroursodeoxycholic acid (TUDCA). Moreover, LcS treatment exhibited a suppressive effect on the hydroxylated primary bile acids α-muricholic acid (α-MCA) and β-muricholic acid (β-MCA). We further demonstrated that LcS treatment suppressed the expression of pro-inflammatory mediators interferon-gamma (IFN-γ) and nitric oxide (NO), and increased the expression of the anti-inflammatory mediator interleukin-10 (IL-10) in colon tissues, potentially as a result of altered bile acid profiles. Mechanistically, we showed that LcS treatment suppressed the activation of nuclear factor-kappa B (NF-κB) signaling via stabilization of inhibitor of NF-κB alpha (IκBα). Altogether, we have demonstrated the therapeutic effects of LcS in DSS-induced colitis, providing new insights into its effect on bile acid metabolism and the related anti-inflammatory mechanisms. Our findings provide support for the application of LcS in the treatment of IBD. |
| first_indexed | 2024-12-10T13:32:11Z |
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| id | doaj.art-3a5345817358430f8443f2b3061a6b27 |
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| publishDate | 2022-04-01 |
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| series | Frontiers in Nutrition |
| spelling | doaj.art-3a5345817358430f8443f2b3061a6b272022-12-22T01:46:56ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2022-04-01910.3389/fnut.2022.816836816836Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBαWing-Yan Wong0Wing-Yan Wong1Brandon Dow Chan2Brandon Dow Chan3Tung-Ting Sham4Magnolia Muk-Lan Lee5Magnolia Muk-Lan Lee6Chi-On Chan7Chi-On Chan8Chung-Ting Chau9Daniel Kam-Wah Mok10Daniel Kam-Wah Mok11Daniel Kam-Wah Mok12Yiu-Wa Kwan13William Chi-Shing Tai14William Chi-Shing Tai15William Chi-Shing Tai16William Chi-Shing Tai17Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaThe Laboratory for Probiotic and Prebiotic Research in Human Health, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaThe Laboratory for Probiotic and Prebiotic Research in Human Health, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaThe Laboratory for Probiotic and Prebiotic Research in Human Health, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaState Key Laboratory of Chinese Medicine and Molecular Pharmacology (Incubation), Shenzhen Research Institute, The Hong Kong Polytechnic University, Shenzhen, ChinaSchool of Biomedical Sciences, The Chinese University of Hong Kong, Sha Tin, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaState Key Laboratory of Chinese Medicine and Molecular Pharmacology (Incubation), Shenzhen Research Institute, The Hong Kong Polytechnic University, Shenzhen, ChinaResearch Institute for Future Food, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaSchool of Biomedical Sciences, The Chinese University of Hong Kong, Sha Tin, Hong Kong SAR, ChinaDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaThe Laboratory for Probiotic and Prebiotic Research in Human Health, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaState Key Laboratory of Chinese Medicine and Molecular Pharmacology (Incubation), Shenzhen Research Institute, The Hong Kong Polytechnic University, Shenzhen, ChinaResearch Institute for Future Food, The Hong Kong Polytechnic University, Hung Hom, Hong Kong SAR, ChinaInflammatory bowel disease (IBD) is a chronic progressive intestinal inflammatory disease, characterized by an altered gut microbiota composition and accompanying alterations in circulatory bile acids. Increasing evidence supports the beneficial effect of probiotics intake on health. Introduction of probiotics to the intestines can modulate gut microbiota composition and in turn regulate the host immune system and modify the inflammatory response. Probiotics can also improve intestinal barrier function and exhibit a positive impact on host physiological and pathological conditions via gut microbiota-derived metabolites. Previous studies have demonstrated that Lactobacillus casei strain Shirota (LcS) treatment could inhibit clinical manifestation of colitis in dextran sulfate sodium (DSS)-induced mice, however, the underlying mechanisms remain unknown. In this study, we employed the DSS-induced acute colitis mouse model to investigate the anti-inflammatory effects of LcS and related mechanisms. Administration of LcS ameliorated the severity of DSS-induced colitis and enhanced intestinal integrity via induction of mucin-2 and occludin expression in colons. Fecal microbiota analysis showed that LcS increased the relative abundance of beneficial bacterial species in colitic mice, whereas the relative abundance of pathobionts was reduced. Additionally, LcS treatment modulated circulating bile acid profiles in colitic mice. In mice treated with LcS, we identified increased levels of primary taurine-conjugated bile acids, including taurocholic acid (TCA) and taurochenodeoxycholic acid (TCDCA). LcS treatment also increased the levels of secondary taurine-conjugated bile acids, including taurodeoxycholic acid (TDCA) and tauroursodeoxycholic acid (TUDCA). Moreover, LcS treatment exhibited a suppressive effect on the hydroxylated primary bile acids α-muricholic acid (α-MCA) and β-muricholic acid (β-MCA). We further demonstrated that LcS treatment suppressed the expression of pro-inflammatory mediators interferon-gamma (IFN-γ) and nitric oxide (NO), and increased the expression of the anti-inflammatory mediator interleukin-10 (IL-10) in colon tissues, potentially as a result of altered bile acid profiles. Mechanistically, we showed that LcS treatment suppressed the activation of nuclear factor-kappa B (NF-κB) signaling via stabilization of inhibitor of NF-κB alpha (IκBα). Altogether, we have demonstrated the therapeutic effects of LcS in DSS-induced colitis, providing new insights into its effect on bile acid metabolism and the related anti-inflammatory mechanisms. Our findings provide support for the application of LcS in the treatment of IBD.https://www.frontiersin.org/articles/10.3389/fnut.2022.816836/fullprobioticsinflammatory bowel diseaseLactobacillus casei strain Shirotagut microbiotabile acidsDSS-induced acute colitis |
| spellingShingle | Wing-Yan Wong Wing-Yan Wong Brandon Dow Chan Brandon Dow Chan Tung-Ting Sham Magnolia Muk-Lan Lee Magnolia Muk-Lan Lee Chi-On Chan Chi-On Chan Chung-Ting Chau Daniel Kam-Wah Mok Daniel Kam-Wah Mok Daniel Kam-Wah Mok Yiu-Wa Kwan William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai William Chi-Shing Tai Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα Frontiers in Nutrition probiotics inflammatory bowel disease Lactobacillus casei strain Shirota gut microbiota bile acids DSS-induced acute colitis |
| title | Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα |
| title_full | Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα |
| title_fullStr | Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα |
| title_full_unstemmed | Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα |
| title_short | Lactobacillus casei Strain Shirota Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice by Increasing Taurine-Conjugated Bile Acids and Inhibiting NF-κB Signaling via Stabilization of IκBα |
| title_sort | lactobacillus casei strain shirota ameliorates dextran sulfate sodium induced colitis in mice by increasing taurine conjugated bile acids and inhibiting nf κb signaling via stabilization of iκbα |
| topic | probiotics inflammatory bowel disease Lactobacillus casei strain Shirota gut microbiota bile acids DSS-induced acute colitis |
| url | https://www.frontiersin.org/articles/10.3389/fnut.2022.816836/full |
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