Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice

Abstract Background Mesenteric adipose tissue (mAT) hyperplasia, known as creeping fat is a pathologic characteristic of Crohn’s disease (CD). The reserve of creeping fat in surgery is associated with poor prognosis of CD patients, but the mechanism remains unknown. Methods Mesenteric microbiome, me...

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Autores principales: Zhen He, Jinjie Wu, Junli Gong, Jia Ke, Tao Ding, Wenjing Zhao, Wai Ming Cheng, Zhanhao Luo, Qilang He, Wanyi Zeng, Jing Yu, Na Jiao, Yanmin Liu, Bin Zheng, Lei Dai, Min Zhi, Xiaojian Wu, Christian Jobin, Ping Lan
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Publicado: BMC 2021
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spelling oai:doaj.org-article:886ce1d62c4a44c99fd819c6704b86892021-11-28T12:08:14ZMicrobiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice10.1186/s40168-021-01178-82049-2618https://doaj.org/article/886ce1d62c4a44c99fd819c6704b86892021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01178-8https://doaj.org/toc/2049-2618Abstract Background Mesenteric adipose tissue (mAT) hyperplasia, known as creeping fat is a pathologic characteristic of Crohn’s disease (CD). The reserve of creeping fat in surgery is associated with poor prognosis of CD patients, but the mechanism remains unknown. Methods Mesenteric microbiome, metabolome, and host transcriptome were characterized using a cohort of 48 patients with CD and 16 non-CD controls. Multidimensional data including 16S ribosomal RNA gene sequencing (16S rRNA), host RNA sequencing, and metabolome were integrated to reveal network interaction. Mesenteric resident bacteria were isolated from mAT and functionally investigated both in the dextran sulfate sodium (DSS) model and in the Il10 gene-deficient (Il10 −/−) mouse colitis model to validate their pro-inflammatory roles. Results Mesenteric microbiota contributed to aberrant metabolites production and transcripts in mATs from patients with CD. The presence of mAT resident microbiota was associated with the development of CD. Achromobacter pulmonis (A. pulmonis) isolated from CD mAT could translocate to mAT and exacerbate both DSS-induced and Il10 gene-deficient (Il10 −/−) spontaneous colitis in mice. The levels of A. pulmonis in both mAT and mucous layer from CD patients were higher compared to those from the non-CD group. Conclusions This study suggests that the mesenteric microbiota from patients with CD sculpt a detrimental microenvironment and promote intestinal inflammation. Video abstractZhen HeJinjie WuJunli GongJia KeTao DingWenjing ZhaoWai Ming ChengZhanhao LuoQilang HeWanyi ZengJing YuNa JiaoYanmin LiuBin ZhengLei DaiMin ZhiXiaojian WuChristian JobinPing LanBMCarticleCrohn’s diseaseMicrobiotaMesenteric adipose tissueBacterial translocationMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-14 (2021)
institution DOAJ
collection DOAJ
language EN
topic Crohn’s disease
Microbiota
Mesenteric adipose tissue
Bacterial translocation
Microbial ecology
QR100-130
spellingShingle Crohn’s disease
Microbiota
Mesenteric adipose tissue
Bacterial translocation
Microbial ecology
QR100-130
Zhen He
Jinjie Wu
Junli Gong
Jia Ke
Tao Ding
Wenjing Zhao
Wai Ming Cheng
Zhanhao Luo
Qilang He
Wanyi Zeng
Jing Yu
Na Jiao
Yanmin Liu
Bin Zheng
Lei Dai
Min Zhi
Xiaojian Wu
Christian Jobin
Ping Lan
Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
description Abstract Background Mesenteric adipose tissue (mAT) hyperplasia, known as creeping fat is a pathologic characteristic of Crohn’s disease (CD). The reserve of creeping fat in surgery is associated with poor prognosis of CD patients, but the mechanism remains unknown. Methods Mesenteric microbiome, metabolome, and host transcriptome were characterized using a cohort of 48 patients with CD and 16 non-CD controls. Multidimensional data including 16S ribosomal RNA gene sequencing (16S rRNA), host RNA sequencing, and metabolome were integrated to reveal network interaction. Mesenteric resident bacteria were isolated from mAT and functionally investigated both in the dextran sulfate sodium (DSS) model and in the Il10 gene-deficient (Il10 −/−) mouse colitis model to validate their pro-inflammatory roles. Results Mesenteric microbiota contributed to aberrant metabolites production and transcripts in mATs from patients with CD. The presence of mAT resident microbiota was associated with the development of CD. Achromobacter pulmonis (A. pulmonis) isolated from CD mAT could translocate to mAT and exacerbate both DSS-induced and Il10 gene-deficient (Il10 −/−) spontaneous colitis in mice. The levels of A. pulmonis in both mAT and mucous layer from CD patients were higher compared to those from the non-CD group. Conclusions This study suggests that the mesenteric microbiota from patients with CD sculpt a detrimental microenvironment and promote intestinal inflammation. Video abstract
format article
author Zhen He
Jinjie Wu
Junli Gong
Jia Ke
Tao Ding
Wenjing Zhao
Wai Ming Cheng
Zhanhao Luo
Qilang He
Wanyi Zeng
Jing Yu
Na Jiao
Yanmin Liu
Bin Zheng
Lei Dai
Min Zhi
Xiaojian Wu
Christian Jobin
Ping Lan
author_facet Zhen He
Jinjie Wu
Junli Gong
Jia Ke
Tao Ding
Wenjing Zhao
Wai Ming Cheng
Zhanhao Luo
Qilang He
Wanyi Zeng
Jing Yu
Na Jiao
Yanmin Liu
Bin Zheng
Lei Dai
Min Zhi
Xiaojian Wu
Christian Jobin
Ping Lan
author_sort Zhen He
title Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
title_short Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
title_full Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
title_fullStr Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
title_full_unstemmed Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
title_sort microbiota in mesenteric adipose tissue from crohn’s disease promote colitis in mice
publisher BMC
publishDate 2021
url https://doaj.org/article/886ce1d62c4a44c99fd819c6704b8689
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