Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation
The relationship between inflammatory bowel disease and sleep disturbances is complicated and of increasing interest. We investigated the inflammatory and immunological consequences of EA in sleep-deprived colitis and found that dextran sulfate sodium (DSS)-induced colitis in sleep-fragmented (SF) m...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-06-01
|
| Series: | Biology |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-7737/11/7/962 |
| _version_ | 1797407430429114368 |
|---|---|
| author | Geng-Hao Liu Xin-Cheng Zhuo Yueh-Hsiang Huang Hsuan-Miao Liu Ren-Chin Wu Chia-Jung Kuo Ning-Hung Chen Li-Pang Chuang Shih-Wei Lin Yen-Lung Chen Huang-Yu Yang Tzung-Yan Lee |
| author_facet | Geng-Hao Liu Xin-Cheng Zhuo Yueh-Hsiang Huang Hsuan-Miao Liu Ren-Chin Wu Chia-Jung Kuo Ning-Hung Chen Li-Pang Chuang Shih-Wei Lin Yen-Lung Chen Huang-Yu Yang Tzung-Yan Lee |
| author_sort | Geng-Hao Liu |
| collection | DOAJ |
| description | The relationship between inflammatory bowel disease and sleep disturbances is complicated and of increasing interest. We investigated the inflammatory and immunological consequences of EA in sleep-deprived colitis and found that dextran sulfate sodium (DSS)-induced colitis in sleep-fragmented (SF) mice was more severe than that in mice with normal sleep. This increase in the severity of colitis was accompanied by reduced body weight, shortened colon length, and deteriorated disease activity index. DSS with SF mice presented obvious diminished intestinal tight junction proteins (claudin-1 and occludin), elevated proinflammatory cytokines (CRP, IFN-γ, IL-6), lowered melatonin and adiponectin levels, downregulated vasoactive intestinal peptide (VIP) type 1 and 2 receptor (VPAC1, VPAC2) expression, and decreased diversity of gut bacteria. EA ameliorated colitis severity and preserved the performance of the epithelial tight junction proteins and VIP receptors, especially VPAC2. Meanwhile, the innate lymphoid cells-derived cytokines in both group 2 (IL-4, IL5, IL-9, IL-13) and group 3 (IL-22, GM-CSF) were elevated in mice colon tissue. Furthermore, dysbiosis was confirmed in the DSS group with and without SF, and EA could maintain the species diversity. <i>Firmicutes</i> could be restored, such as <i>Lachnospiraceae</i>, and <i>Proteobacteria</i> become rebalanced, mainly <i>Enterobacteriaceae</i>, after EA intervention. On the other hand, SF plays different roles in physiological and pathological conditions. In normal mice, interrupted sleep did not affect the expression of claudin-1 and occludin. But VPAC1, VPAC2, and gut microbiota diversity, including <i>Burkholderiaceae</i> and <i>Rhodococcus</i>, were opposite to mice in an inflamed state. |
| first_indexed | 2024-03-09T03:41:22Z |
| format | Article |
| id | doaj.art-4d97cb9b4b2b4681a34018c575a627a5 |
| institution | Directory Open Access Journal |
| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-09T03:41:22Z |
| publishDate | 2022-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Biology |
| spelling | doaj.art-4d97cb9b4b2b4681a34018c575a627a52023-12-03T14:40:21ZengMDPI AGBiology2079-77372022-06-0111796210.3390/biology11070962Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep FragmentationGeng-Hao Liu0Xin-Cheng Zhuo1Yueh-Hsiang Huang2Hsuan-Miao Liu3Ren-Chin Wu4Chia-Jung Kuo5Ning-Hung Chen6Li-Pang Chuang7Shih-Wei Lin8Yen-Lung Chen9Huang-Yu Yang10Tzung-Yan Lee11School of Traditional Chinese Medicine, College of Medicine, Chang Gung University, Taoyuan 333323, TaiwanDepartment of General Medicine, Taipei Medical University Hospital, Taipei 110301, TaiwanDivision of Chinese Internal Medicine, Center for Traditional Chinese Medicine, Chang Gung Memorial Hospital, Taipei 105406, TaiwanGraduate Institute of Traditional Chinese Medicine, School of Traditional Chinese Medicine, College of Medicine, Chang Gung University, Taoyuan 333323, TaiwanSchool of Traditional Chinese Medicine, College of Medicine, Chang Gung University, Taoyuan 333323, TaiwanDepartment of Gastroenterology and Hepatology, Linkou Chang Gung Memorial Hospital, Taoyuan 333423, TaiwanSchool of Traditional Chinese Medicine, College of Medicine, Chang Gung University, Taoyuan 333323, TaiwanSleep Center, Chang Gung Memorial Hospital, Taoyuan 333008, TaiwanSleep Center, Chang Gung Memorial Hospital, Taoyuan 333008, TaiwanDivision of Acupuncture and Moxibustion, Center for Traditional Chinese Medicine, Chang Gung Memorial Hospital, Taoyuan 333423, TaiwanDepartment of Nephrology, Linkou Chang Gung Memorial Hospital, Taoyuan 333423, TaiwanGraduate Institute of Traditional Chinese Medicine, School of Traditional Chinese Medicine, College of Medicine, Chang Gung University, Taoyuan 333323, TaiwanThe relationship between inflammatory bowel disease and sleep disturbances is complicated and of increasing interest. We investigated the inflammatory and immunological consequences of EA in sleep-deprived colitis and found that dextran sulfate sodium (DSS)-induced colitis in sleep-fragmented (SF) mice was more severe than that in mice with normal sleep. This increase in the severity of colitis was accompanied by reduced body weight, shortened colon length, and deteriorated disease activity index. DSS with SF mice presented obvious diminished intestinal tight junction proteins (claudin-1 and occludin), elevated proinflammatory cytokines (CRP, IFN-γ, IL-6), lowered melatonin and adiponectin levels, downregulated vasoactive intestinal peptide (VIP) type 1 and 2 receptor (VPAC1, VPAC2) expression, and decreased diversity of gut bacteria. EA ameliorated colitis severity and preserved the performance of the epithelial tight junction proteins and VIP receptors, especially VPAC2. Meanwhile, the innate lymphoid cells-derived cytokines in both group 2 (IL-4, IL5, IL-9, IL-13) and group 3 (IL-22, GM-CSF) were elevated in mice colon tissue. Furthermore, dysbiosis was confirmed in the DSS group with and without SF, and EA could maintain the species diversity. <i>Firmicutes</i> could be restored, such as <i>Lachnospiraceae</i>, and <i>Proteobacteria</i> become rebalanced, mainly <i>Enterobacteriaceae</i>, after EA intervention. On the other hand, SF plays different roles in physiological and pathological conditions. In normal mice, interrupted sleep did not affect the expression of claudin-1 and occludin. But VPAC1, VPAC2, and gut microbiota diversity, including <i>Burkholderiaceae</i> and <i>Rhodococcus</i>, were opposite to mice in an inflamed state.https://www.mdpi.com/2079-7737/11/7/962inflammatory bowel disease (IBD)sleep fragmentationelectroacupunctureST36intestinal tight junctiongut microbiota |
| spellingShingle | Geng-Hao Liu Xin-Cheng Zhuo Yueh-Hsiang Huang Hsuan-Miao Liu Ren-Chin Wu Chia-Jung Kuo Ning-Hung Chen Li-Pang Chuang Shih-Wei Lin Yen-Lung Chen Huang-Yu Yang Tzung-Yan Lee Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation Biology inflammatory bowel disease (IBD) sleep fragmentation electroacupuncture ST36 intestinal tight junction gut microbiota |
| title | Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation |
| title_full | Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation |
| title_fullStr | Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation |
| title_full_unstemmed | Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation |
| title_short | Alterations in Gut Microbiota and Upregulations of VPAC2 and Intestinal Tight Junctions Correlate with Anti-Inflammatory Effects of Electroacupuncture in Colitis Mice with Sleep Fragmentation |
| title_sort | alterations in gut microbiota and upregulations of vpac2 and intestinal tight junctions correlate with anti inflammatory effects of electroacupuncture in colitis mice with sleep fragmentation |
| topic | inflammatory bowel disease (IBD) sleep fragmentation electroacupuncture ST36 intestinal tight junction gut microbiota |
| url | https://www.mdpi.com/2079-7737/11/7/962 |
| work_keys_str_mv | AT genghaoliu alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT xinchengzhuo alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT yuehhsianghuang alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT hsuanmiaoliu alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT renchinwu alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT chiajungkuo alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT ninghungchen alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT lipangchuang alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT shihweilin alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT yenlungchen alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT huangyuyang alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation AT tzungyanlee alterationsingutmicrobiotaandupregulationsofvpac2andintestinaltightjunctionscorrelatewithantiinflammatoryeffectsofelectroacupunctureincolitismicewithsleepfragmentation |