Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics
Patients with ulcerative colitis (UC) have a high prevalence of mental disorders, such as depression and anxiety. Gut microbiota imbalance and disturbed metabolism have been suggested to play an important role in either UC or mental disorders. However, little is known about their detailed multi-omic...
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Taylor & Francis Group
2021
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oai:doaj.org-article:578d94d6d1b5472db20e8f346ad58a172021-11-26T11:19:48ZDepression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics1949-09761949-098410.1080/19490976.2021.1987779https://doaj.org/article/578d94d6d1b5472db20e8f346ad58a172021-01-01T00:00:00Zhttp://dx.doi.org/10.1080/19490976.2021.1987779https://doaj.org/toc/1949-0976https://doaj.org/toc/1949-0984Patients with ulcerative colitis (UC) have a high prevalence of mental disorders, such as depression and anxiety. Gut microbiota imbalance and disturbed metabolism have been suggested to play an important role in either UC or mental disorders. However, little is known about their detailed multi-omics characteristics in patients with UC and depression/anxiety. In this prospective observational study, 240 Chinese patients were enrolled, including 129 patients with active UC (69 in Phase 1 and 60 in Phase 2; divided into depression/non-depression or anxiety/non-anxiety groups), 49 patients with depression and anxiety (non-UC), and 62 healthy people. The gut microbiota of all subjects was analyzed using 16S rRNA sequencing. The serum metabolome and proteome of patients with UC in Phase 2 were analyzed using liquid chromatography/mass spectrometry. Associations between multi-omics were evaluated by correlation analysis. The prophylactic effect of candidate metabolites on the depressive-like behavior of mice with colitis was investigated. In total, 58% of patients with active UC had depression, while 50% had anxiety. Compared to patients with UC without depression/anxiety, patients with UC and depression/anxiety had lower fecal microbial community richness and diversity, with more Lactobacillales, Sellimonas, Streptococcus, and Enterococcus but less Prevotella_9 and Lachnospira. Most metabolites (e.g., glycochenodeoxycholate) were increased in the serum, while few metabolites, including 2ʹ-deoxy-D-ribose and L-pipecolic acid, were decreased, accompanied by a general reduction in immunoglobulin proteins. These related bacteria, metabolites, and proteins were highly connected. A prophylactic administration of 2ʹ-deoxy-D-ribose and L-pipecolic acid significantly reduced the depressive-like behaviors in mice with colitis and alleviated the inflammatory cytokine levels in their colon, blood and brain. This study has identified a comprehensive multi-omics network related to depression and anxiety in active UC. It is composed of a certain set of gut microbiota, metabolites, and proteins, which are potential targets for clinical intervention for patients with UC and depression/anxiety.Xiaomin YuanBiqing ChenZhenglan DuanZiqian XiaYang DingTuo ChenHuize LiuBaosheng WangBolin YangXiaoyong WangShijia LiuJin-Yong ZhouYajun LiuQiong WangZhaofeng ShenJun XiaoHongtao ShangWeiwei LiuGuoping ShiLei ZhuYugen ChenTaylor & Francis Grouparticleulcerative colitismicrobiota-gut-brain axismulti-omics analysesDiseases of the digestive system. GastroenterologyRC799-869ENGut Microbes, Vol 13, Iss 1 (2021) |
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| topic |
ulcerative colitis microbiota-gut-brain axis multi-omics analyses Diseases of the digestive system. Gastroenterology RC799-869 |
| spellingShingle |
ulcerative colitis microbiota-gut-brain axis multi-omics analyses Diseases of the digestive system. Gastroenterology RC799-869 Xiaomin Yuan Biqing Chen Zhenglan Duan Ziqian Xia Yang Ding Tuo Chen Huize Liu Baosheng Wang Bolin Yang Xiaoyong Wang Shijia Liu Jin-Yong Zhou Yajun Liu Qiong Wang Zhaofeng Shen Jun Xiao Hongtao Shang Weiwei Liu Guoping Shi Lei Zhu Yugen Chen Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| description |
Patients with ulcerative colitis (UC) have a high prevalence of mental disorders, such as depression and anxiety. Gut microbiota imbalance and disturbed metabolism have been suggested to play an important role in either UC or mental disorders. However, little is known about their detailed multi-omics characteristics in patients with UC and depression/anxiety. In this prospective observational study, 240 Chinese patients were enrolled, including 129 patients with active UC (69 in Phase 1 and 60 in Phase 2; divided into depression/non-depression or anxiety/non-anxiety groups), 49 patients with depression and anxiety (non-UC), and 62 healthy people. The gut microbiota of all subjects was analyzed using 16S rRNA sequencing. The serum metabolome and proteome of patients with UC in Phase 2 were analyzed using liquid chromatography/mass spectrometry. Associations between multi-omics were evaluated by correlation analysis. The prophylactic effect of candidate metabolites on the depressive-like behavior of mice with colitis was investigated. In total, 58% of patients with active UC had depression, while 50% had anxiety. Compared to patients with UC without depression/anxiety, patients with UC and depression/anxiety had lower fecal microbial community richness and diversity, with more Lactobacillales, Sellimonas, Streptococcus, and Enterococcus but less Prevotella_9 and Lachnospira. Most metabolites (e.g., glycochenodeoxycholate) were increased in the serum, while few metabolites, including 2ʹ-deoxy-D-ribose and L-pipecolic acid, were decreased, accompanied by a general reduction in immunoglobulin proteins. These related bacteria, metabolites, and proteins were highly connected. A prophylactic administration of 2ʹ-deoxy-D-ribose and L-pipecolic acid significantly reduced the depressive-like behaviors in mice with colitis and alleviated the inflammatory cytokine levels in their colon, blood and brain. This study has identified a comprehensive multi-omics network related to depression and anxiety in active UC. It is composed of a certain set of gut microbiota, metabolites, and proteins, which are potential targets for clinical intervention for patients with UC and depression/anxiety. |
| format |
article |
| author |
Xiaomin Yuan Biqing Chen Zhenglan Duan Ziqian Xia Yang Ding Tuo Chen Huize Liu Baosheng Wang Bolin Yang Xiaoyong Wang Shijia Liu Jin-Yong Zhou Yajun Liu Qiong Wang Zhaofeng Shen Jun Xiao Hongtao Shang Weiwei Liu Guoping Shi Lei Zhu Yugen Chen |
| author_facet |
Xiaomin Yuan Biqing Chen Zhenglan Duan Ziqian Xia Yang Ding Tuo Chen Huize Liu Baosheng Wang Bolin Yang Xiaoyong Wang Shijia Liu Jin-Yong Zhou Yajun Liu Qiong Wang Zhaofeng Shen Jun Xiao Hongtao Shang Weiwei Liu Guoping Shi Lei Zhu Yugen Chen |
| author_sort |
Xiaomin Yuan |
| title |
Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| title_short |
Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| title_full |
Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| title_fullStr |
Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| title_full_unstemmed |
Depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| title_sort |
depression and anxiety in patients with active ulcerative colitis: crosstalk of gut microbiota, metabolomics and proteomics |
| publisher |
Taylor & Francis Group |
| publishDate |
2021 |
| url |
https://doaj.org/article/578d94d6d1b5472db20e8f346ad58a17 |
| work_keys_str_mv |
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