Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation

Abstract Complement component C3 mediates pathology in CNS neurodegenerative diseases. Here we use scRNAseq of sorted C3-reporter positive cells from mouse brain and optic nerve to characterize C3 producing glia in experimental autoimmune encephalomyelitis (EAE), a model in which peripheral immune c...

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Main Authors: Thomas Garton, Matthew D. Smith, Ajay Kesharwani, Marjan Gharagozloo, Sungtaek Oh, Chan-Hyun Na, Martina Absinta, Daniel S. Reich, Donald J. Zack, Peter A. Calabresi
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58708-3
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author Thomas Garton
Matthew D. Smith
Ajay Kesharwani
Marjan Gharagozloo
Sungtaek Oh
Chan-Hyun Na
Martina Absinta
Daniel S. Reich
Donald J. Zack
Peter A. Calabresi
author_facet Thomas Garton
Matthew D. Smith
Ajay Kesharwani
Marjan Gharagozloo
Sungtaek Oh
Chan-Hyun Na
Martina Absinta
Daniel S. Reich
Donald J. Zack
Peter A. Calabresi
author_sort Thomas Garton
collection DOAJ
description Abstract Complement component C3 mediates pathology in CNS neurodegenerative diseases. Here we use scRNAseq of sorted C3-reporter positive cells from mouse brain and optic nerve to characterize C3 producing glia in experimental autoimmune encephalomyelitis (EAE), a model in which peripheral immune cells infiltrate the CNS, causing reactive gliosis and neuro-axonal pathology. We find that C3 expression in the early inflammatory stage of EAE defines disease-associated glial subtypes characterized by increased expression of genes associated with mTOR activation and cell metabolism. This pro-inflammatory subtype is abrogated with genetic C3 depletion, a finding confirmed with proteomic analyses. In addition, early optic nerve axonal injury and retinal ganglion cell oxidative stress, but not loss of post-synaptic density protein 95, are ameliorated by selective deletion of C3 in myeloid cells. These data suggest that in addition to C3b opsonization of post synaptic proteins leading to neuronal demise, C3 activation is a contributor to reactive glia in the optic nerve.
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spelling doaj-art-b063adbcb1694e969f0b539475015a2f2025-08-20T02:12:06ZengNature PortfolioNature Communications2041-17232025-04-0116112110.1038/s41467-025-58708-3Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammationThomas Garton0Matthew D. Smith1Ajay Kesharwani2Marjan Gharagozloo3Sungtaek Oh4Chan-Hyun Na5Martina Absinta6Daniel S. Reich7Donald J. Zack8Peter A. Calabresi9Department of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineDepartment of Ophthalmology, Wilmer Eye Institute, Johns Hopkins University School of MedicineDepartment of Neurology, Johns Hopkins University School of MedicineAbstract Complement component C3 mediates pathology in CNS neurodegenerative diseases. Here we use scRNAseq of sorted C3-reporter positive cells from mouse brain and optic nerve to characterize C3 producing glia in experimental autoimmune encephalomyelitis (EAE), a model in which peripheral immune cells infiltrate the CNS, causing reactive gliosis and neuro-axonal pathology. We find that C3 expression in the early inflammatory stage of EAE defines disease-associated glial subtypes characterized by increased expression of genes associated with mTOR activation and cell metabolism. This pro-inflammatory subtype is abrogated with genetic C3 depletion, a finding confirmed with proteomic analyses. In addition, early optic nerve axonal injury and retinal ganglion cell oxidative stress, but not loss of post-synaptic density protein 95, are ameliorated by selective deletion of C3 in myeloid cells. These data suggest that in addition to C3b opsonization of post synaptic proteins leading to neuronal demise, C3 activation is a contributor to reactive glia in the optic nerve.https://doi.org/10.1038/s41467-025-58708-3
spellingShingle Thomas Garton
Matthew D. Smith
Ajay Kesharwani
Marjan Gharagozloo
Sungtaek Oh
Chan-Hyun Na
Martina Absinta
Daniel S. Reich
Donald J. Zack
Peter A. Calabresi
Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
Nature Communications
title Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
title_full Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
title_fullStr Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
title_full_unstemmed Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
title_short Myeloid lineage C3 induces reactive gliosis and neuronal stress during CNS inflammation
title_sort myeloid lineage c3 induces reactive gliosis and neuronal stress during cns inflammation
url https://doi.org/10.1038/s41467-025-58708-3
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