Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation

Abstract Background Aflatoxin B1 (AFB1) is a mycotoxin that widely found in the environment and mouldy foods. AFB1 initially targets the intestine, and AFB1-induced intestinal injury cannot be ignored. Lactobacillus amylovorus (LA), a predominant species of Lactobacillus, plays a role in carbohydrat...

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Main Authors: Jinyan Li, Mengdie Shi, Yubo Wang, Jinyan Liu, Shuiping Liu, Weili Kang, Xianjiao Liu, Xingxiang Chen, Kehe Huang, Yunhuan Liu
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Journal of Nanobiotechnology
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Online Access:https://doi.org/10.1186/s12951-024-02979-3
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author Jinyan Li
Mengdie Shi
Yubo Wang
Jinyan Liu
Shuiping Liu
Weili Kang
Xianjiao Liu
Xingxiang Chen
Kehe Huang
Yunhuan Liu
author_facet Jinyan Li
Mengdie Shi
Yubo Wang
Jinyan Liu
Shuiping Liu
Weili Kang
Xianjiao Liu
Xingxiang Chen
Kehe Huang
Yunhuan Liu
author_sort Jinyan Li
collection DOAJ
description Abstract Background Aflatoxin B1 (AFB1) is a mycotoxin that widely found in the environment and mouldy foods. AFB1 initially targets the intestine, and AFB1-induced intestinal injury cannot be ignored. Lactobacillus amylovorus (LA), a predominant species of Lactobacillus, plays a role in carbohydrate metabolism. Extracellular vesicles (EVs), small lipid membrane vesicles, are widely involved in diverse cellular processes. However, the mechanism by which Lactobacillus amylovorus-QC1H-derived EVs (LA.EVs) protect against AFB1-induced intestinal injury remains unclear. Results In our study, a new strain named Lactobacillus amylovorus-QC1H (LA-QC1H) was isolated from pig faeces. Then, EVs derived from LA-QC1H were extracted via ultracentrifugation. Our results showed that LA.EVs significantly alleviated AFB1-induced intestinal injury by inhibiting the production of proinflammatory cytokines, decreasing intestinal permeability and increasing the expression of tight junction proteins. Moreover, 16 S rRNA analysis revealed that LA.EVs modulated AFB1-induced gut dysbiosis in mice. However, LA.EVs did not exert beneficial effects in antibiotic-treated mice. LA.EVs treatment increased intestinal levels of indole-3-acetic acid (IAA) and activated intestinal aryl hydrocarbon receptor (AHR)/interleukin-22 (IL-22) signalling in AFB1-exposed mice. Inhibition of intestinal AHR signalling markedly weakened the protective effect of LA.EVs in AFB1-exposed mice. Conclusions LA.EVs alleviated AFB1-induced intestinal injury by modulating the gut microbiota, activating the intestinal AHR/IL-22 signalling, reducing the inflammatory response and promoting intestinal barrier repair in mice.
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spelling doaj-art-df29bd948c094f21be456c25454d466e2024-11-17T12:47:07ZengBMCJournal of Nanobiotechnology1477-31552024-11-0122111910.1186/s12951-024-02979-3Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activationJinyan Li0Mengdie Shi1Yubo Wang2Jinyan Liu3Shuiping Liu4Weili Kang5Xianjiao Liu6Xingxiang Chen7Kehe Huang8Yunhuan Liu9College of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Veterinary Medicine, Nanjing Agricultural UniversityAbstract Background Aflatoxin B1 (AFB1) is a mycotoxin that widely found in the environment and mouldy foods. AFB1 initially targets the intestine, and AFB1-induced intestinal injury cannot be ignored. Lactobacillus amylovorus (LA), a predominant species of Lactobacillus, plays a role in carbohydrate metabolism. Extracellular vesicles (EVs), small lipid membrane vesicles, are widely involved in diverse cellular processes. However, the mechanism by which Lactobacillus amylovorus-QC1H-derived EVs (LA.EVs) protect against AFB1-induced intestinal injury remains unclear. Results In our study, a new strain named Lactobacillus amylovorus-QC1H (LA-QC1H) was isolated from pig faeces. Then, EVs derived from LA-QC1H were extracted via ultracentrifugation. Our results showed that LA.EVs significantly alleviated AFB1-induced intestinal injury by inhibiting the production of proinflammatory cytokines, decreasing intestinal permeability and increasing the expression of tight junction proteins. Moreover, 16 S rRNA analysis revealed that LA.EVs modulated AFB1-induced gut dysbiosis in mice. However, LA.EVs did not exert beneficial effects in antibiotic-treated mice. LA.EVs treatment increased intestinal levels of indole-3-acetic acid (IAA) and activated intestinal aryl hydrocarbon receptor (AHR)/interleukin-22 (IL-22) signalling in AFB1-exposed mice. Inhibition of intestinal AHR signalling markedly weakened the protective effect of LA.EVs in AFB1-exposed mice. Conclusions LA.EVs alleviated AFB1-induced intestinal injury by modulating the gut microbiota, activating the intestinal AHR/IL-22 signalling, reducing the inflammatory response and promoting intestinal barrier repair in mice.https://doi.org/10.1186/s12951-024-02979-3Aflatoxin B1Lactobacillus amylovorusExtracellular vesiclesGut microbiotaAryl hydrocarbon receptor
spellingShingle Jinyan Li
Mengdie Shi
Yubo Wang
Jinyan Liu
Shuiping Liu
Weili Kang
Xianjiao Liu
Xingxiang Chen
Kehe Huang
Yunhuan Liu
Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
Journal of Nanobiotechnology
Aflatoxin B1
Lactobacillus amylovorus
Extracellular vesicles
Gut microbiota
Aryl hydrocarbon receptor
title Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
title_full Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
title_fullStr Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
title_full_unstemmed Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
title_short Probiotic-derived extracellular vesicles alleviate AFB1-induced intestinal injury by modulating the gut microbiota and AHR activation
title_sort probiotic derived extracellular vesicles alleviate afb1 induced intestinal injury by modulating the gut microbiota and ahr activation
topic Aflatoxin B1
Lactobacillus amylovorus
Extracellular vesicles
Gut microbiota
Aryl hydrocarbon receptor
url https://doi.org/10.1186/s12951-024-02979-3
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