Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet

Metabolic endotoxemia originating from dysbiotic gut microbiota has been identified as a primary mediator for triggering the chronic low-grade inflammation (CLGI) responsible for the development of obesity. Capsaicin (CAP) is the major pungent bioactivator in chili peppers and has potent anti-obesit...

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Main Authors: Chao Kang, Bin Wang, Kanakaraju Kaliannan, Xiaolan Wang, Hedong Lang, Suocheng Hui, Li Huang, Yong Zhang, Ming Zhou, Mengting Chen, Mantian Mi, Filipa Godoy-Vitorino, Maria Gloria Dominguez Bello
Format: Article
Language:English
Published: American Society for Microbiology 2017-05-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/8/3/e00470-17
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spelling doaj-93557d2d5afa4b1c83e62e1d878a31cb2021-07-02T02:08:17ZengAmerican Society for MicrobiologymBio2150-75112017-05-0183e00470-1710.1128/mBio.00470-17Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat DietChao KangBin WangKanakaraju KaliannanXiaolan WangHedong LangSuocheng HuiLi HuangYong ZhangMing ZhouMengting ChenMantian MiFilipa Godoy-VitorinoMaria Gloria Dominguez BelloMetabolic endotoxemia originating from dysbiotic gut microbiota has been identified as a primary mediator for triggering the chronic low-grade inflammation (CLGI) responsible for the development of obesity. Capsaicin (CAP) is the major pungent bioactivator in chili peppers and has potent anti-obesity functions, yet the mechanisms linking this effect to gut microbiota remain obscure. Here we show that mice fed a high-fat diet (HFD) supplemented with CAP exhibit lower levels of metabolic endotoxemia and CLGI associated with lower body weight gain. High-resolution responses of the microbiota were examined by 16S rRNA sequencing, short-chain fatty acid (SCFA) measurements, and phylogenetic reconstruction of unobserved states (PICRUSt) analysis. The results showed, among others, that dietary CAP induced increased levels of butyrate-producing Ruminococcaceae and Lachnospiraceae, while it caused lower levels of members of the lipopolysaccharide (LPS)-producing family S24_7. Predicted function analysis (PICRUSt) showed depletion of genes involved in bacterial LPS synthesis in response to CAP. We further identified that inhibition of cannabinoid receptor type 1 (CB1) by CAP also contributes to prevention of HFD-induced gut barrier dysfunction. Importantly, fecal microbiota transplantation experiments conducted in germfree mice demonstrated that dietary CAP-induced protection against HFD-induced obesity is transferrable. Moreover, microbiota depletion by a cocktail of antibiotics was sufficient to block the CAP-induced protective phenotype against obesity, further suggesting the role of microbiota in this context. Together, our findings uncover an interaction between dietary CAP and gut microbiota as a novel mechanism for the anti-obesity effect of CAP acting through prevention of microbial dysbiosis, gut barrier dysfunction, and chronic low-grade inflammation.http://mbio.asm.org/cgi/content/full/8/3/e00470-17
collection DOAJ
language English
format Article
sources DOAJ
author Chao Kang
Bin Wang
Kanakaraju Kaliannan
Xiaolan Wang
Hedong Lang
Suocheng Hui
Li Huang
Yong Zhang
Ming Zhou
Mengting Chen
Mantian Mi
Filipa Godoy-Vitorino
Maria Gloria Dominguez Bello
spellingShingle Chao Kang
Bin Wang
Kanakaraju Kaliannan
Xiaolan Wang
Hedong Lang
Suocheng Hui
Li Huang
Yong Zhang
Ming Zhou
Mengting Chen
Mantian Mi
Filipa Godoy-Vitorino
Maria Gloria Dominguez Bello
Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
mBio
author_facet Chao Kang
Bin Wang
Kanakaraju Kaliannan
Xiaolan Wang
Hedong Lang
Suocheng Hui
Li Huang
Yong Zhang
Ming Zhou
Mengting Chen
Mantian Mi
Filipa Godoy-Vitorino
Maria Gloria Dominguez Bello
author_sort Chao Kang
title Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
title_short Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
title_full Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
title_fullStr Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
title_full_unstemmed Gut Microbiota Mediates the Protective Effects of Dietary Capsaicin against Chronic Low-Grade Inflammation and Associated Obesity Induced by High-Fat Diet
title_sort gut microbiota mediates the protective effects of dietary capsaicin against chronic low-grade inflammation and associated obesity induced by high-fat diet
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2017-05-01
description Metabolic endotoxemia originating from dysbiotic gut microbiota has been identified as a primary mediator for triggering the chronic low-grade inflammation (CLGI) responsible for the development of obesity. Capsaicin (CAP) is the major pungent bioactivator in chili peppers and has potent anti-obesity functions, yet the mechanisms linking this effect to gut microbiota remain obscure. Here we show that mice fed a high-fat diet (HFD) supplemented with CAP exhibit lower levels of metabolic endotoxemia and CLGI associated with lower body weight gain. High-resolution responses of the microbiota were examined by 16S rRNA sequencing, short-chain fatty acid (SCFA) measurements, and phylogenetic reconstruction of unobserved states (PICRUSt) analysis. The results showed, among others, that dietary CAP induced increased levels of butyrate-producing Ruminococcaceae and Lachnospiraceae, while it caused lower levels of members of the lipopolysaccharide (LPS)-producing family S24_7. Predicted function analysis (PICRUSt) showed depletion of genes involved in bacterial LPS synthesis in response to CAP. We further identified that inhibition of cannabinoid receptor type 1 (CB1) by CAP also contributes to prevention of HFD-induced gut barrier dysfunction. Importantly, fecal microbiota transplantation experiments conducted in germfree mice demonstrated that dietary CAP-induced protection against HFD-induced obesity is transferrable. Moreover, microbiota depletion by a cocktail of antibiotics was sufficient to block the CAP-induced protective phenotype against obesity, further suggesting the role of microbiota in this context. Together, our findings uncover an interaction between dietary CAP and gut microbiota as a novel mechanism for the anti-obesity effect of CAP acting through prevention of microbial dysbiosis, gut barrier dysfunction, and chronic low-grade inflammation.
url http://mbio.asm.org/cgi/content/full/8/3/e00470-17
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