Gut microbes–spinal connection is required for itch sensation

The gut microbiota has been linked to a number of neurological disorders. However, it is unclear whether the gut microbiota is involved in the genesis of chronic itch, a refractory condition that afflicts patients both physically and mentally. Here, we report that depletion of gut microbiota enhance...

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Main Authors: Tong Jin, Si-Yuan Li, Hong-Li Zheng, Xiao-Dan Liu, Yue Huang, Gan Ma, Ya-Xuan Zhao, Xiao-Tian Zhao, Li Yang, Qi-Hui Wang, Hong-Jun Wang, Chengyong Gu, Zhiqiang Pan, Fuqing Lin
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2025.2495859
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author Tong Jin
Si-Yuan Li
Hong-Li Zheng
Xiao-Dan Liu
Yue Huang
Gan Ma
Ya-Xuan Zhao
Xiao-Tian Zhao
Li Yang
Qi-Hui Wang
Hong-Jun Wang
Chengyong Gu
Zhiqiang Pan
Fuqing Lin
author_facet Tong Jin
Si-Yuan Li
Hong-Li Zheng
Xiao-Dan Liu
Yue Huang
Gan Ma
Ya-Xuan Zhao
Xiao-Tian Zhao
Li Yang
Qi-Hui Wang
Hong-Jun Wang
Chengyong Gu
Zhiqiang Pan
Fuqing Lin
author_sort Tong Jin
collection DOAJ
description The gut microbiota has been linked to a number of neurological disorders. However, it is unclear whether the gut microbiota is involved in the genesis of chronic itch, a refractory condition that afflicts patients both physically and mentally. Here, we report that depletion of gut microbiota enhances tolerance to itch in mice orally administered with antibiotics (ABX) and mice free of germ. Of note, oral gavage with Bacteroides fragilis (B. fragilis), a prominent species of the genus Bacteroides with most differential change, corrected the ABX-induced itch dysfunction through its driven metabolite acetyl-l-carnitine (ALC). Mechanistically, gut microbiota or B. fragilis depletion caused a decrease in RNA N6-methyladenosine (m6A) demethylase FTO expression in the dorsal horn and a consequent increase in RNA m6A sites in Mas-related G protein-coupled receptor F (MrgprF) mRNA, leading to decreased MRGPRF protein. The downregulation of FTO was triggered by inactivation of ETS proto-oncogene 1 (ETS1), a transcription factor that binds to the Fto promoter. These findings support a gut microbe – spinal connection in modulation of itch sensation in RNA m6A epigenetic-dependent manner and highlight a critical role of ALC in linking the altered B. fragilis and itch dysfunction.
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spelling doaj-art-0e045c73b0ed40ea819d51746335c7fd2025-08-20T02:20:05ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2495859Gut microbes–spinal connection is required for itch sensationTong Jin0Si-Yuan Li1Hong-Li Zheng2Xiao-Dan Liu3Yue Huang4Gan Ma5Ya-Xuan Zhao6Xiao-Tian Zhao7Li Yang8Qi-Hui Wang9Hong-Jun Wang10Chengyong Gu11Zhiqiang Pan12Fuqing Lin13Jiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaAnesthesiology Department, Suzhou Municipal Hospital, Nanjing Medical University Affiliated Suzhou Hospital, Suzhou, ChinaJiangsu Province Key Laboratory of Anesthesiology, Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical University, Xuzhou, ChinaDepartment of Pain, Shanghai Tenth People’s Hospital, School of Medicine, Tongji University, Shanghai, ChinaThe gut microbiota has been linked to a number of neurological disorders. However, it is unclear whether the gut microbiota is involved in the genesis of chronic itch, a refractory condition that afflicts patients both physically and mentally. Here, we report that depletion of gut microbiota enhances tolerance to itch in mice orally administered with antibiotics (ABX) and mice free of germ. Of note, oral gavage with Bacteroides fragilis (B. fragilis), a prominent species of the genus Bacteroides with most differential change, corrected the ABX-induced itch dysfunction through its driven metabolite acetyl-l-carnitine (ALC). Mechanistically, gut microbiota or B. fragilis depletion caused a decrease in RNA N6-methyladenosine (m6A) demethylase FTO expression in the dorsal horn and a consequent increase in RNA m6A sites in Mas-related G protein-coupled receptor F (MrgprF) mRNA, leading to decreased MRGPRF protein. The downregulation of FTO was triggered by inactivation of ETS proto-oncogene 1 (ETS1), a transcription factor that binds to the Fto promoter. These findings support a gut microbe – spinal connection in modulation of itch sensation in RNA m6A epigenetic-dependent manner and highlight a critical role of ALC in linking the altered B. fragilis and itch dysfunction.https://www.tandfonline.com/doi/10.1080/19490976.2025.2495859Gut microbeitchFTORNA m6AB. fragilisacetyl-l-carnitine
spellingShingle Tong Jin
Si-Yuan Li
Hong-Li Zheng
Xiao-Dan Liu
Yue Huang
Gan Ma
Ya-Xuan Zhao
Xiao-Tian Zhao
Li Yang
Qi-Hui Wang
Hong-Jun Wang
Chengyong Gu
Zhiqiang Pan
Fuqing Lin
Gut microbes–spinal connection is required for itch sensation
Gut Microbes
Gut microbe
itch
FTO
RNA m6A
B. fragilis
acetyl-l-carnitine
title Gut microbes–spinal connection is required for itch sensation
title_full Gut microbes–spinal connection is required for itch sensation
title_fullStr Gut microbes–spinal connection is required for itch sensation
title_full_unstemmed Gut microbes–spinal connection is required for itch sensation
title_short Gut microbes–spinal connection is required for itch sensation
title_sort gut microbes spinal connection is required for itch sensation
topic Gut microbe
itch
FTO
RNA m6A
B. fragilis
acetyl-l-carnitine
url https://www.tandfonline.com/doi/10.1080/19490976.2025.2495859
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