Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway

Abstract RhoA, a small GTPase, plays a pivotal role in various diseases, including spinal cord injury (SCI). Although RhoA inhibition has been traditionally viewed as beneficial for SCI repair, recent clinical trials of RhoA inhibitors in SCI have failed to show significant therapeutic efficacy, sug...

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Main Authors: Jiale Cai, Xinya Zheng, Xiongbo Luo, Wenli Cui, Xinrui Ma, Shuyi Xu, Lanya Fu, Jiaqi Zhang, Yizhou Xu, Yunlun Li, Ye He, Xianghai Wang, Jiasong Guo
Format: Article
Language:English
Published: Nature Publishing Group 2025-08-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07947-9
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author Jiale Cai
Xinya Zheng
Xiongbo Luo
Wenli Cui
Xinrui Ma
Shuyi Xu
Lanya Fu
Jiaqi Zhang
Yizhou Xu
Yunlun Li
Ye He
Xianghai Wang
Jiasong Guo
author_facet Jiale Cai
Xinya Zheng
Xiongbo Luo
Wenli Cui
Xinrui Ma
Shuyi Xu
Lanya Fu
Jiaqi Zhang
Yizhou Xu
Yunlun Li
Ye He
Xianghai Wang
Jiasong Guo
author_sort Jiale Cai
collection DOAJ
description Abstract RhoA, a small GTPase, plays a pivotal role in various diseases, including spinal cord injury (SCI). Although RhoA inhibition has been traditionally viewed as beneficial for SCI repair, recent clinical trials of RhoA inhibitors in SCI have failed to show significant therapeutic efficacy, suggesting functional heterogeneity across different cell types. The role of RhoA in microglia, the key immune cells involve in SCI, remains poorly understood. Using microglial RhoA conditional knockout mice, this study demonstrated that RhoA deficiency in microglia attenuates the morphological and functional repair of the SCI mice, and impairs the microglial biofunctions of proliferation, phagocytosis, and migration. Single-cell RNA sequencing, bulk RNA sequencing, and metabolomics revealed that RhoA deficiency can attenuate the microglial glycolytic enzyme expression, ATP production, ECAR and OCR levels through the Arhgap25/HIF-1α pathway. Overall, this is the first study to demonstrate that microglial RhoA is essential for SCI repair, the Arhgap25/HIF-1α pathway mediated glucose metabolism might enlighten a novel insight to enrich the understanding on the complex roles of RhoA and microglia in SCI repair. Moreover, this study highlights the importance of considering cell-specific roles of RhoA in SCI repair and provides a foundation for developing targeted therapies aimed at microglial metabolic reprogramming. Schematic representation of the proposed mechanism by which microglial RhoA regulates glycolytic adaptation and spinal cord repair. (Created by Figdraw.com with permission of # wgq=r7c74c).
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issn 2041-4889
language English
publishDate 2025-08-01
publisher Nature Publishing Group
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series Cell Death and Disease
spelling doaj-art-e04c0b6208b0496b8449ab0452cd1d062025-08-24T11:54:32ZengNature Publishing GroupCell Death and Disease2041-48892025-08-0116111410.1038/s41419-025-07947-9Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathwayJiale Cai0Xinya Zheng1Xiongbo Luo2Wenli Cui3Xinrui Ma4Shuyi Xu5Lanya Fu6Jiaqi Zhang7Yizhou Xu8Yunlun Li9Ye He10Xianghai Wang11Jiasong Guo12Department of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityDepartment of Histology and Embryology, Guangdong Provincial Key Laboratory of Construction and Detection in Tissue Engineering, National Demonstration Center for Experimental Education, School of Basic Medical Sciences, Department of Neurosurgery, Institute of Brain Diseases, Nanfang Hospital, Southern Medical UniversityAbstract RhoA, a small GTPase, plays a pivotal role in various diseases, including spinal cord injury (SCI). Although RhoA inhibition has been traditionally viewed as beneficial for SCI repair, recent clinical trials of RhoA inhibitors in SCI have failed to show significant therapeutic efficacy, suggesting functional heterogeneity across different cell types. The role of RhoA in microglia, the key immune cells involve in SCI, remains poorly understood. Using microglial RhoA conditional knockout mice, this study demonstrated that RhoA deficiency in microglia attenuates the morphological and functional repair of the SCI mice, and impairs the microglial biofunctions of proliferation, phagocytosis, and migration. Single-cell RNA sequencing, bulk RNA sequencing, and metabolomics revealed that RhoA deficiency can attenuate the microglial glycolytic enzyme expression, ATP production, ECAR and OCR levels through the Arhgap25/HIF-1α pathway. Overall, this is the first study to demonstrate that microglial RhoA is essential for SCI repair, the Arhgap25/HIF-1α pathway mediated glucose metabolism might enlighten a novel insight to enrich the understanding on the complex roles of RhoA and microglia in SCI repair. Moreover, this study highlights the importance of considering cell-specific roles of RhoA in SCI repair and provides a foundation for developing targeted therapies aimed at microglial metabolic reprogramming. Schematic representation of the proposed mechanism by which microglial RhoA regulates glycolytic adaptation and spinal cord repair. (Created by Figdraw.com with permission of # wgq=r7c74c).https://doi.org/10.1038/s41419-025-07947-9
spellingShingle Jiale Cai
Xinya Zheng
Xiongbo Luo
Wenli Cui
Xinrui Ma
Shuyi Xu
Lanya Fu
Jiaqi Zhang
Yizhou Xu
Yunlun Li
Ye He
Xianghai Wang
Jiasong Guo
Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
Cell Death and Disease
title Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
title_full Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
title_fullStr Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
title_full_unstemmed Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
title_short Loss of RhoA in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through Arhgap25/HIF-1α pathway
title_sort loss of rhoa in microglia disables glycolytic adaptation and impairs spinal cord injury recovery through arhgap25 hif 1α pathway
url https://doi.org/10.1038/s41419-025-07947-9
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