Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.

Gut microbiota play an important part in the pathogenesis of mucosal inflammation, such as inflammatory bowel disease (IBD). However, owing to the complexity of the gut microbiota, our understanding of the roles of commensal and pathogenic bacteria in the maintenance of immune homeostasis in the gut...

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Main Authors: Chil-Sung Kang, Mingi Ban, Eun-Jeong Choi, Hyung-Geun Moon, Jun-Sung Jeon, Dae-Kyum Kim, Soo-Kyung Park, Seong Gyu Jeon, Tae-Young Roh, Seung-Jae Myung, Yong Song Gho, Jae Gyu Kim, Yoon-Keun Kim
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3811976?pdf=render
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spelling doaj-a34523c49cc44ab790722fb7ce1641992020-11-25T02:44:21ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-01810e7652010.1371/journal.pone.0076520Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.Chil-Sung KangMingi BanEun-Jeong ChoiHyung-Geun MoonJun-Sung JeonDae-Kyum KimSoo-Kyung ParkSeong Gyu JeonTae-Young RohSeung-Jae MyungYong Song GhoJae Gyu KimYoon-Keun KimGut microbiota play an important part in the pathogenesis of mucosal inflammation, such as inflammatory bowel disease (IBD). However, owing to the complexity of the gut microbiota, our understanding of the roles of commensal and pathogenic bacteria in the maintenance of immune homeostasis in the gut is evolving only slowly. Here, we evaluated the role of gut microbiota and their secreting extracellular vesicles (EV) in the development of mucosal inflammation in the gut. Experimental IBD model was established by oral application of dextran sulfate sodium (DSS) to C57BL/6 mice. The composition of gut microbiota and bacteria-derived EV in stools was evaluated by metagenome sequencing using bacterial common primer of 16S rDNA. Metagenomics in the IBD mouse model showed that the change in stool EV composition was more drastic, compared to the change of bacterial composition. Oral DSS application decreased the composition of EV from Akkermansia muciniphila and Bacteroides acidifaciens in stools, whereas increased EV from TM7 phylum, especially from species DQ777900_s and AJ400239_s. In vitro pretreatment of A. muciniphila-derived EV ameliorated the production of a pro-inflammatory cytokine IL-6 from colon epithelial cells induced by Escherichia coli EV. Additionally, oral application of A. muciniphila EV also protected DSS-induced IBD phenotypes, such as body weight loss, colon length, and inflammatory cell infiltration of colon wall. Our data provides insight into the role of gut microbiota-derived EV in regulation of intestinal immunity and homeostasis, and A. muciniphila-derived EV have protective effects in the development of DSS-induced colitis.http://europepmc.org/articles/PMC3811976?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Chil-Sung Kang
Mingi Ban
Eun-Jeong Choi
Hyung-Geun Moon
Jun-Sung Jeon
Dae-Kyum Kim
Soo-Kyung Park
Seong Gyu Jeon
Tae-Young Roh
Seung-Jae Myung
Yong Song Gho
Jae Gyu Kim
Yoon-Keun Kim
spellingShingle Chil-Sung Kang
Mingi Ban
Eun-Jeong Choi
Hyung-Geun Moon
Jun-Sung Jeon
Dae-Kyum Kim
Soo-Kyung Park
Seong Gyu Jeon
Tae-Young Roh
Seung-Jae Myung
Yong Song Gho
Jae Gyu Kim
Yoon-Keun Kim
Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
PLoS ONE
author_facet Chil-Sung Kang
Mingi Ban
Eun-Jeong Choi
Hyung-Geun Moon
Jun-Sung Jeon
Dae-Kyum Kim
Soo-Kyung Park
Seong Gyu Jeon
Tae-Young Roh
Seung-Jae Myung
Yong Song Gho
Jae Gyu Kim
Yoon-Keun Kim
author_sort Chil-Sung Kang
title Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
title_short Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
title_full Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
title_fullStr Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
title_full_unstemmed Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
title_sort extracellular vesicles derived from gut microbiota, especially akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Gut microbiota play an important part in the pathogenesis of mucosal inflammation, such as inflammatory bowel disease (IBD). However, owing to the complexity of the gut microbiota, our understanding of the roles of commensal and pathogenic bacteria in the maintenance of immune homeostasis in the gut is evolving only slowly. Here, we evaluated the role of gut microbiota and their secreting extracellular vesicles (EV) in the development of mucosal inflammation in the gut. Experimental IBD model was established by oral application of dextran sulfate sodium (DSS) to C57BL/6 mice. The composition of gut microbiota and bacteria-derived EV in stools was evaluated by metagenome sequencing using bacterial common primer of 16S rDNA. Metagenomics in the IBD mouse model showed that the change in stool EV composition was more drastic, compared to the change of bacterial composition. Oral DSS application decreased the composition of EV from Akkermansia muciniphila and Bacteroides acidifaciens in stools, whereas increased EV from TM7 phylum, especially from species DQ777900_s and AJ400239_s. In vitro pretreatment of A. muciniphila-derived EV ameliorated the production of a pro-inflammatory cytokine IL-6 from colon epithelial cells induced by Escherichia coli EV. Additionally, oral application of A. muciniphila EV also protected DSS-induced IBD phenotypes, such as body weight loss, colon length, and inflammatory cell infiltration of colon wall. Our data provides insight into the role of gut microbiota-derived EV in regulation of intestinal immunity and homeostasis, and A. muciniphila-derived EV have protective effects in the development of DSS-induced colitis.
url http://europepmc.org/articles/PMC3811976?pdf=render
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