Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats
Abstract Background Gut microbial dysbiosis and gut-brain axis dysfunction have been implicated in the pathophysiology of migraine. However, it is unclear whether migraine-related cephalic allodynia could induce the alteration of gut microbial composition. Methods A classic migraine rat model was es...
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| Format: | Article |
| Language: | English |
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BMC
2022-06-01
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| Series: | The Journal of Headache and Pain |
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| Online Access: | https://doi.org/10.1186/s10194-022-01441-9 |
| _version_ | 1818250229397323776 |
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| author | Shuai Miao Wenjing Tang Heng Li Bozhi Li Chunxiao Yang Wei Xie Tao Wang Wenhao Bai Zihua Gong Zhao Dong Shengyuan Yu |
| author_facet | Shuai Miao Wenjing Tang Heng Li Bozhi Li Chunxiao Yang Wei Xie Tao Wang Wenhao Bai Zihua Gong Zhao Dong Shengyuan Yu |
| author_sort | Shuai Miao |
| collection | DOAJ |
| description | Abstract Background Gut microbial dysbiosis and gut-brain axis dysfunction have been implicated in the pathophysiology of migraine. However, it is unclear whether migraine-related cephalic allodynia could induce the alteration of gut microbial composition. Methods A classic migraine rat model was established by repeated dural infusions of inflammatory soup (IS). Periorbital mechanical threshold and nociception-related behaviors were used to evaluate IS-induced cephalic allodynia and the preventive effect of topiramate. The alterations in gut microbial composition and potential metabolic pathways were investigated based on the results of 16 S rRNA gene sequencing. Microbiota-related short-chain fatty acids and tryptophan metabolites were detected and quantified by mass spectrometry analysis. Results Repeated dural IS infusions induced cephalic allodynia (decreased mechanical threshold), migraine-like behaviors (increased immobility time and reduced moving distance), and microbial composition alteration, which were ameliorated by the treatment of topiramate. Decreased Lactobacillus was the most prominent biomarker genus in the IS-induced alteration of microbial composition. Additionally, IS infusions also enhanced metabolic pathways of the gut microbiota in butanoate, propanoate, and tryptophan, while the increased tryptophan-related metabolites indole-3-acetamide and tryptophol in feces could be the indicators. Conclusions Inflammatory dural stimulation-induced cephalic allodynia causes the alterations of gut microbiota profile and microbial metabolic pathways. |
| first_indexed | 2024-12-12T15:49:04Z |
| format | Article |
| id | doaj.art-c3a05e0ec6d445eab66ca86bb043de40 |
| institution | Directory Open Access Journal |
| issn | 1129-2369 1129-2377 |
| language | English |
| last_indexed | 2024-12-12T15:49:04Z |
| publishDate | 2022-06-01 |
| publisher | BMC |
| record_format | Article |
| series | The Journal of Headache and Pain |
| spelling | doaj.art-c3a05e0ec6d445eab66ca86bb043de402022-12-22T00:19:40ZengBMCThe Journal of Headache and Pain1129-23691129-23772022-06-0123111310.1186/s10194-022-01441-9Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in ratsShuai Miao0Wenjing Tang1Heng Li2Bozhi Li3Chunxiao Yang4Wei Xie5Tao Wang6Wenhao Bai7Zihua Gong8Zhao Dong9Shengyuan Yu10Department of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, The First Affiliated Hospital of Shandong First Medical UniversityDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalDepartment of Neurology, the First Medical Center, Chinese PLA General HospitalAbstract Background Gut microbial dysbiosis and gut-brain axis dysfunction have been implicated in the pathophysiology of migraine. However, it is unclear whether migraine-related cephalic allodynia could induce the alteration of gut microbial composition. Methods A classic migraine rat model was established by repeated dural infusions of inflammatory soup (IS). Periorbital mechanical threshold and nociception-related behaviors were used to evaluate IS-induced cephalic allodynia and the preventive effect of topiramate. The alterations in gut microbial composition and potential metabolic pathways were investigated based on the results of 16 S rRNA gene sequencing. Microbiota-related short-chain fatty acids and tryptophan metabolites were detected and quantified by mass spectrometry analysis. Results Repeated dural IS infusions induced cephalic allodynia (decreased mechanical threshold), migraine-like behaviors (increased immobility time and reduced moving distance), and microbial composition alteration, which were ameliorated by the treatment of topiramate. Decreased Lactobacillus was the most prominent biomarker genus in the IS-induced alteration of microbial composition. Additionally, IS infusions also enhanced metabolic pathways of the gut microbiota in butanoate, propanoate, and tryptophan, while the increased tryptophan-related metabolites indole-3-acetamide and tryptophol in feces could be the indicators. Conclusions Inflammatory dural stimulation-induced cephalic allodynia causes the alterations of gut microbiota profile and microbial metabolic pathways.https://doi.org/10.1186/s10194-022-01441-9MigraineCephalic allodyniaGut microbiota16 S rRNA gene sequencingGut-brain axis |
| spellingShingle | Shuai Miao Wenjing Tang Heng Li Bozhi Li Chunxiao Yang Wei Xie Tao Wang Wenhao Bai Zihua Gong Zhao Dong Shengyuan Yu Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats The Journal of Headache and Pain Migraine Cephalic allodynia Gut microbiota 16 S rRNA gene sequencing Gut-brain axis |
| title | Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats |
| title_full | Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats |
| title_fullStr | Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats |
| title_full_unstemmed | Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats |
| title_short | Repeated inflammatory dural stimulation-induced cephalic allodynia causes alteration of gut microbial composition in rats |
| title_sort | repeated inflammatory dural stimulation induced cephalic allodynia causes alteration of gut microbial composition in rats |
| topic | Migraine Cephalic allodynia Gut microbiota 16 S rRNA gene sequencing Gut-brain axis |
| url | https://doi.org/10.1186/s10194-022-01441-9 |
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