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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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) |
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Crohn’s disease Microbiota Mesenteric adipose tissue Bacterial translocation Microbial ecology QR100-130 |
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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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