Dicer deficiency affects microglial function during demyelination and impairs remyelination

Microglia are essential regulators of central nervous system (CNS) homeostasis, playing key roles in demyelination and remyelination. Dysregulated microglial activity contributes to pathological inflammation and impaired repair processes in demyelinating diseases. Here, we investigate the role of Di...

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Main Authors: Ajai Tripathi, Nagendra Kumar Rai, Aaron Perles, Haley Courtney, Claire Jones, Adya Sapra, Jason Plemel, Ranjan Dutta
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Neurobiology of Disease
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Online Access:http://www.sciencedirect.com/science/article/pii/S0969996125000956
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author Ajai Tripathi
Nagendra Kumar Rai
Aaron Perles
Haley Courtney
Claire Jones
Adya Sapra
Jason Plemel
Ranjan Dutta
author_facet Ajai Tripathi
Nagendra Kumar Rai
Aaron Perles
Haley Courtney
Claire Jones
Adya Sapra
Jason Plemel
Ranjan Dutta
author_sort Ajai Tripathi
collection DOAJ
description Microglia are essential regulators of central nervous system (CNS) homeostasis, playing key roles in demyelination and remyelination. Dysregulated microglial activity contributes to pathological inflammation and impaired repair processes in demyelinating diseases. Here, we investigate the role of Dicer1, a critical enzyme in microRNA biogenesis, in affecting microglial function, demyelination, and remyelination. Loss of Dicer1 in microglia resulted in amplified inflammatory responses, defective myelin debris clearance, and disruption of metabolic homeostasis, leading to exacerbated demyelination and delayed remyelination. Transcriptomic analysis revealed significant upregulation of inflammatory pathways, including interferon signaling and JAK/STAT activation, alongside a loss of homeostatic microglial gene expression. Protein-level validation confirmed sustained secretion of pro-inflammatory cytokines such as IFN-γ, IL-16, and CXCL12, creating a chronic inflammatory environment that impaired remyelination. Furthermore, Dicer1-deficient microglia failed to support oligodendrocyte progenitor cells (OPCs) differentiation/maturation, with increased apoptosis of mature oligodendrocytes (OLs), contributing to remyelination failure. These findings identify Dicer1 as a critical regulator of microglial homeostasis and inflammation resolution, highlighting its potential as a therapeutic target to mitigate inflammation and promote repair in demyelinating diseases.
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spelling doaj-art-e20ae64bce0b43b2ae85a260f15d5d0f2025-08-20T02:16:27ZengElsevierNeurobiology of Disease1095-953X2025-05-0120810687910.1016/j.nbd.2025.106879Dicer deficiency affects microglial function during demyelination and impairs remyelinationAjai Tripathi0Nagendra Kumar Rai1Aaron Perles2Haley Courtney3Claire Jones4Adya Sapra5Jason Plemel6Ranjan Dutta7Department of Neurosciences, Cleveland Clinic, Cleveland, OH, USADepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USADepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USADepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USADepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USADepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USANeuroscience and Mental Health Institute, Department of Medicine, Division of Neurology, Department of Medical Microbiology and Immunology, University of Alberta, CanadaDepartment of Neurosciences, Cleveland Clinic, Cleveland, OH, USA; Cleveland Clinic Lerner College of Medicine, Cleveland, OH, USA; Corresponding author at: Department of Neurosciences, Lerner Research Institute, Cleveland Clinic, 9500 Euclid Avenue/ NC30, Cleveland, OH 44195, USA.Microglia are essential regulators of central nervous system (CNS) homeostasis, playing key roles in demyelination and remyelination. Dysregulated microglial activity contributes to pathological inflammation and impaired repair processes in demyelinating diseases. Here, we investigate the role of Dicer1, a critical enzyme in microRNA biogenesis, in affecting microglial function, demyelination, and remyelination. Loss of Dicer1 in microglia resulted in amplified inflammatory responses, defective myelin debris clearance, and disruption of metabolic homeostasis, leading to exacerbated demyelination and delayed remyelination. Transcriptomic analysis revealed significant upregulation of inflammatory pathways, including interferon signaling and JAK/STAT activation, alongside a loss of homeostatic microglial gene expression. Protein-level validation confirmed sustained secretion of pro-inflammatory cytokines such as IFN-γ, IL-16, and CXCL12, creating a chronic inflammatory environment that impaired remyelination. Furthermore, Dicer1-deficient microglia failed to support oligodendrocyte progenitor cells (OPCs) differentiation/maturation, with increased apoptosis of mature oligodendrocytes (OLs), contributing to remyelination failure. These findings identify Dicer1 as a critical regulator of microglial homeostasis and inflammation resolution, highlighting its potential as a therapeutic target to mitigate inflammation and promote repair in demyelinating diseases.http://www.sciencedirect.com/science/article/pii/S0969996125000956MicrogliaDicer1microRNACytokinesInflammationDemyelination
spellingShingle Ajai Tripathi
Nagendra Kumar Rai
Aaron Perles
Haley Courtney
Claire Jones
Adya Sapra
Jason Plemel
Ranjan Dutta
Dicer deficiency affects microglial function during demyelination and impairs remyelination
Neurobiology of Disease
Microglia
Dicer1
microRNA
Cytokines
Inflammation
Demyelination
title Dicer deficiency affects microglial function during demyelination and impairs remyelination
title_full Dicer deficiency affects microglial function during demyelination and impairs remyelination
title_fullStr Dicer deficiency affects microglial function during demyelination and impairs remyelination
title_full_unstemmed Dicer deficiency affects microglial function during demyelination and impairs remyelination
title_short Dicer deficiency affects microglial function during demyelination and impairs remyelination
title_sort dicer deficiency affects microglial function during demyelination and impairs remyelination
topic Microglia
Dicer1
microRNA
Cytokines
Inflammation
Demyelination
url http://www.sciencedirect.com/science/article/pii/S0969996125000956
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