Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain
Chemotherapy-induced peripheral neuropathy (CIPN) and its related pain are common challenges for patients receiving oxaliplatin chemotherapy. Oxaliplatin accumulation in dorsal root ganglion (DRGs) is known to impair gene transcription by epigenetic dysregulation. We hypothesized that sodium butyrat...
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| Language: | English |
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Elsevier
2025-01-01
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| Series: | Neurotherapeutics |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1878747924001685 |
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| author | Idy H.T. Ho Yidan Zou Kele Luo Fenfen Qin Yanjun Jiang Qian Li Tingting Jin Xinyi Zhang Huarong Chen Likai Tan Lin Zhang Tony Gin William K.K. Wu Matthew T.V. Chan Changyu Jiang Xiaodong Liu |
| author_facet | Idy H.T. Ho Yidan Zou Kele Luo Fenfen Qin Yanjun Jiang Qian Li Tingting Jin Xinyi Zhang Huarong Chen Likai Tan Lin Zhang Tony Gin William K.K. Wu Matthew T.V. Chan Changyu Jiang Xiaodong Liu |
| author_sort | Idy H.T. Ho |
| collection | DOAJ |
| description | Chemotherapy-induced peripheral neuropathy (CIPN) and its related pain are common challenges for patients receiving oxaliplatin chemotherapy. Oxaliplatin accumulation in dorsal root ganglion (DRGs) is known to impair gene transcription by epigenetic dysregulation. We hypothesized that sodium butyrate, a pro-resolution short-chain fatty acid, inhibited histone acetylation in DRGs and abolished K+ channel dysregulation-induced neuronal hyperexcitability after oxaliplatin treatment. Mechanical allodynia and cold hyperalgesia of mice receiving an accumulation of 15 mg/kg oxaliplatin, with or without intraperitoneal sodium butyrate supplementation, were assessed using von Frey test and acetone evaporation test. Differential expressions of histone deacetylases (HDACs) and pain-related K+ channels were quantified with rt-qPCR and protein assays. Immunofluorescence assays of histone acetylation at H3K9/14 were performed in primary DRG cultures treated with sodium butyrate. Current clamp recording of action potentials and persistent outward current of Twik-related-spinal cord K+ (TRESK) channel were recorded in DRG neurons with small diameters extract. Accompanied by mechanical allodynia and cold hyperalgesia, HDAC1 was upregulated in mice receiving oxaliplatin treatment. Sodium butyrate enhanced global histone acetylation at H3K9/14 in DRG neurons. In vivo sodium butyrate supplementation restored oxaliplatin-induced Kcnj9 and Kcnk18 expression and pain-related behaviors in mice for at least 14 days. Oxaliplatin-induced increase in action potentials frequencies and decrease in magnitudes of KCNK18-related current were reversed in mice receiving sodium butyrate supplementation. This study suggests that sodium butyrate was a useful agent to relieve oxaliplatin-mediated neuropathic pain. |
| format | Article |
| id | doaj-art-21d24b5a9ad444bb9ba0207b7c72155e |
| institution | Kabale University |
| issn | 1878-7479 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurotherapeutics |
| spelling | doaj-art-21d24b5a9ad444bb9ba0207b7c72155e2025-02-01T04:11:52ZengElsevierNeurotherapeutics1878-74792025-01-01221e00481Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic painIdy H.T. Ho0Yidan Zou1Kele Luo2Fenfen Qin3Yanjun Jiang4Qian Li5Tingting Jin6Xinyi Zhang7Huarong Chen8Likai Tan9Lin Zhang10Tony Gin11William K.K. Wu12Matthew T.V. Chan13Changyu Jiang14Xiaodong Liu15Department of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaThe Chinese University of Hong Kong, Shenzhen, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Institute of Digestive Disease, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; State Key Laboratory of Digestive Disease, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaState Key Laboratory of Digestive Disease, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Microbiota I Centre (MagIC), The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; The Chinese University of Hong Kong, Shenzhen, China; State Key Laboratory of Digestive Disease, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, ChinaDepartment of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Corresponding authors.Department of Pain Medicine and Shenzhen Municipal Key Laboratory for Pain Medicine, The 6th Affiliated Hospital of Shenzhen University Medical School, Shenzhen, China; Corresponding authors.Department of Anaesthesia and Intensive Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Peter Hung Pain Research Institute, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China; Corresponding authors.Chemotherapy-induced peripheral neuropathy (CIPN) and its related pain are common challenges for patients receiving oxaliplatin chemotherapy. Oxaliplatin accumulation in dorsal root ganglion (DRGs) is known to impair gene transcription by epigenetic dysregulation. We hypothesized that sodium butyrate, a pro-resolution short-chain fatty acid, inhibited histone acetylation in DRGs and abolished K+ channel dysregulation-induced neuronal hyperexcitability after oxaliplatin treatment. Mechanical allodynia and cold hyperalgesia of mice receiving an accumulation of 15 mg/kg oxaliplatin, with or without intraperitoneal sodium butyrate supplementation, were assessed using von Frey test and acetone evaporation test. Differential expressions of histone deacetylases (HDACs) and pain-related K+ channels were quantified with rt-qPCR and protein assays. Immunofluorescence assays of histone acetylation at H3K9/14 were performed in primary DRG cultures treated with sodium butyrate. Current clamp recording of action potentials and persistent outward current of Twik-related-spinal cord K+ (TRESK) channel were recorded in DRG neurons with small diameters extract. Accompanied by mechanical allodynia and cold hyperalgesia, HDAC1 was upregulated in mice receiving oxaliplatin treatment. Sodium butyrate enhanced global histone acetylation at H3K9/14 in DRG neurons. In vivo sodium butyrate supplementation restored oxaliplatin-induced Kcnj9 and Kcnk18 expression and pain-related behaviors in mice for at least 14 days. Oxaliplatin-induced increase in action potentials frequencies and decrease in magnitudes of KCNK18-related current were reversed in mice receiving sodium butyrate supplementation. This study suggests that sodium butyrate was a useful agent to relieve oxaliplatin-mediated neuropathic pain.http://www.sciencedirect.com/science/article/pii/S1878747924001685Chemotherapy-induced peripheral neuropathyButyrateEpigeneticsHistone deacetylase inhibitionDorsal root ganglion |
| spellingShingle | Idy H.T. Ho Yidan Zou Kele Luo Fenfen Qin Yanjun Jiang Qian Li Tingting Jin Xinyi Zhang Huarong Chen Likai Tan Lin Zhang Tony Gin William K.K. Wu Matthew T.V. Chan Changyu Jiang Xiaodong Liu Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain Neurotherapeutics Chemotherapy-induced peripheral neuropathy Butyrate Epigenetics Histone deacetylase inhibition Dorsal root ganglion |
| title | Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain |
| title_full | Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain |
| title_fullStr | Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain |
| title_full_unstemmed | Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain |
| title_short | Sodium butyrate restored TRESK current controlling neuronal hyperexcitability in a mouse model of oxaliplatin-induced peripheral neuropathic pain |
| title_sort | sodium butyrate restored tresk current controlling neuronal hyperexcitability in a mouse model of oxaliplatin induced peripheral neuropathic pain |
| topic | Chemotherapy-induced peripheral neuropathy Butyrate Epigenetics Histone deacetylase inhibition Dorsal root ganglion |
| url | http://www.sciencedirect.com/science/article/pii/S1878747924001685 |
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