Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis
ABSTRACTMagnitude and diversity of gut microbiota and metabolic systems are critical in shaping human health and diseases, but it remains largely unclear how complex metabolites may selectively regulate gut microbiota and determine health and diseases. Here, we show that failures or compromised effe...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2023-12-01
|
| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2211501 |
| _version_ | 1797236624831021056 |
|---|---|
| author | Yiwei Chen Qiongdan Mai Zixu Chen Tao Lin Yongjie Cai Jing Han Ying Wang Mudan Zhang Shimin Tan Zhiying Wu Lingming Chen Zhiyi Zhang Yi Yang Taimei Cui Beiyin Ouyang Yue Sun Lijia Yang Lin Xu Sien Zhang Jian Li Hongbo Shen Linna Liu Lingchan Zeng Shenghong Zhang Gucheng Zeng |
| author_facet | Yiwei Chen Qiongdan Mai Zixu Chen Tao Lin Yongjie Cai Jing Han Ying Wang Mudan Zhang Shimin Tan Zhiying Wu Lingming Chen Zhiyi Zhang Yi Yang Taimei Cui Beiyin Ouyang Yue Sun Lijia Yang Lin Xu Sien Zhang Jian Li Hongbo Shen Linna Liu Lingchan Zeng Shenghong Zhang Gucheng Zeng |
| author_sort | Yiwei Chen |
| collection | DOAJ |
| description | ABSTRACTMagnitude and diversity of gut microbiota and metabolic systems are critical in shaping human health and diseases, but it remains largely unclear how complex metabolites may selectively regulate gut microbiota and determine health and diseases. Here, we show that failures or compromised effects of anti-TNF-α therapy in inflammatory bowel diseases (IBD) patients were correlated with intestinal dysbacteriosis with more pro-inflammatory bacteria, extensive unresolved inflammation, failed mucosal repairment, and aberrant lipid metabolism, particularly lower levels of palmitoleic acid (POA). Dietary POA repaired gut mucosal barriers, reduced inflammatory cell infiltrations and expressions of TNF-α and IL-6, and improved efficacy of anti-TNF-α therapy in both acute and chronic IBD mouse models. Ex vivo treatment with POA in cultured inflamed colon tissues derived from Crohn’s disease (CD) patients reduced pro-inflammatory signaling/cytokines and conferred appreciable tissue repairment. Mechanistically, POA significantly upregulated the transcriptional signatures of cell division and biosynthetic process of Akkermansia muciniphila, selectively increased the growth and abundance of Akkermansia muciniphila in gut microbiota, and further reprogrammed the composition and structures of gut microbiota. Oral transfer of such POA-reprogrammed, but not control, gut microbiota induced better protection against colitis in anti-TNF-α mAb-treated recipient mice, and co-administration of POA with Akkermansia muciniphila showed significant synergistic protections against colitis in mice. Collectively, this work not only reveals the critical importance of POA as a polyfunctional molecular force to shape the magnitude and diversity of gut microbiota and therefore promote the intestinal homeostasis, but also implicates a new potential therapeutic strategy against intestinal or abenteric inflammatory diseases. |
| first_indexed | 2024-03-11T14:19:54Z |
| format | Article |
| id | doaj.art-039b41385e144351bbc923428eb0f917 |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-24T17:06:49Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-039b41385e144351bbc923428eb0f9172024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2211501Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitisYiwei Chen0Qiongdan Mai1Zixu Chen2Tao Lin3Yongjie Cai4Jing Han5Ying Wang6Mudan Zhang7Shimin Tan8Zhiying Wu9Lingming Chen10Zhiyi Zhang11Yi Yang12Taimei Cui13Beiyin Ouyang14Yue Sun15Lijia Yang16Lin Xu17Sien Zhang18Jian Li19Hongbo Shen20Linna Liu21Lingchan Zeng22Shenghong Zhang23Gucheng Zeng24Department of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDivision of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDivision of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDivision of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaHospital of Stomatology, Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, ChinaCollege of Stomatology, Jinan University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaHospital of Stomatology, Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, ChinaThe Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai, ChinaClinic and Research Center of Tuberculosis, Shanghai Key Laboratory of Tuberculosis, Tongji University Shanghai Pulmonary Hospital, Shanghai, ChinaGuangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, ChinaClinical Research Center, Department of Medical Records Management, Guanghua School of Stomatology, Hospital of Stomatology, Sun Yat-sen University, Guangzhou, ChinaDivision of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaDepartment of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, ChinaABSTRACTMagnitude and diversity of gut microbiota and metabolic systems are critical in shaping human health and diseases, but it remains largely unclear how complex metabolites may selectively regulate gut microbiota and determine health and diseases. Here, we show that failures or compromised effects of anti-TNF-α therapy in inflammatory bowel diseases (IBD) patients were correlated with intestinal dysbacteriosis with more pro-inflammatory bacteria, extensive unresolved inflammation, failed mucosal repairment, and aberrant lipid metabolism, particularly lower levels of palmitoleic acid (POA). Dietary POA repaired gut mucosal barriers, reduced inflammatory cell infiltrations and expressions of TNF-α and IL-6, and improved efficacy of anti-TNF-α therapy in both acute and chronic IBD mouse models. Ex vivo treatment with POA in cultured inflamed colon tissues derived from Crohn’s disease (CD) patients reduced pro-inflammatory signaling/cytokines and conferred appreciable tissue repairment. Mechanistically, POA significantly upregulated the transcriptional signatures of cell division and biosynthetic process of Akkermansia muciniphila, selectively increased the growth and abundance of Akkermansia muciniphila in gut microbiota, and further reprogrammed the composition and structures of gut microbiota. Oral transfer of such POA-reprogrammed, but not control, gut microbiota induced better protection against colitis in anti-TNF-α mAb-treated recipient mice, and co-administration of POA with Akkermansia muciniphila showed significant synergistic protections against colitis in mice. Collectively, this work not only reveals the critical importance of POA as a polyfunctional molecular force to shape the magnitude and diversity of gut microbiota and therefore promote the intestinal homeostasis, but also implicates a new potential therapeutic strategy against intestinal or abenteric inflammatory diseases.https://www.tandfonline.com/doi/10.1080/19490976.2023.2211501Gut microbiotaBiological therapyInflammatory bowel diseasesAkkermansia muciniphilaTNF-α |
| spellingShingle | Yiwei Chen Qiongdan Mai Zixu Chen Tao Lin Yongjie Cai Jing Han Ying Wang Mudan Zhang Shimin Tan Zhiying Wu Lingming Chen Zhiyi Zhang Yi Yang Taimei Cui Beiyin Ouyang Yue Sun Lijia Yang Lin Xu Sien Zhang Jian Li Hongbo Shen Linna Liu Lingchan Zeng Shenghong Zhang Gucheng Zeng Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis Gut Microbes Gut microbiota Biological therapy Inflammatory bowel diseases Akkermansia muciniphila TNF-α |
| title | Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| title_full | Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| title_fullStr | Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| title_full_unstemmed | Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| title_short | Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| title_sort | dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis |
| topic | Gut microbiota Biological therapy Inflammatory bowel diseases Akkermansia muciniphila TNF-α |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2211501 |
| work_keys_str_mv | AT yiweichen dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT qiongdanmai dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT zixuchen dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT taolin dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT yongjiecai dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT jinghan dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT yingwang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT mudanzhang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT shimintan dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT zhiyingwu dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT lingmingchen dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT zhiyizhang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT yiyang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT taimeicui dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT beiyinouyang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT yuesun dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT lijiayang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT linxu dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT sienzhang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT jianli dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT hongboshen dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT linnaliu dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT lingchanzeng dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT shenghongzhang dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis AT guchengzeng dietarypalmitoleicacidreprogramsgutmicrobiotaandimprovesbiologicaltherapyagainstcolitis |