Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation

Autoimmune neuroinflammation occurs when an individual’s immune cells attack the brain, spinal cord or peripheral nerves. Several Suppressor of Cytokine Signaling (SOCS) proteins have been shown to limit pro-inflammatory signaling pathways in myeloid cells and prevent neuroinflammation. They rely on...

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Main Authors: Yohaniz Ortega-Burgos, Asif A. Dar, Siera A. Tomishima, Ipsita Guha, Carleigh O’ Brien, Nadia Porter, F. Chris Bennett, Paula M. Oliver
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-08-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1611818/full
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author Yohaniz Ortega-Burgos
Yohaniz Ortega-Burgos
Asif A. Dar
Siera A. Tomishima
Siera A. Tomishima
Ipsita Guha
Carleigh O’ Brien
Nadia Porter
F. Chris Bennett
F. Chris Bennett
Paula M. Oliver
Paula M. Oliver
author_facet Yohaniz Ortega-Burgos
Yohaniz Ortega-Burgos
Asif A. Dar
Siera A. Tomishima
Siera A. Tomishima
Ipsita Guha
Carleigh O’ Brien
Nadia Porter
F. Chris Bennett
F. Chris Bennett
Paula M. Oliver
Paula M. Oliver
author_sort Yohaniz Ortega-Burgos
collection DOAJ
description Autoimmune neuroinflammation occurs when an individual’s immune cells attack the brain, spinal cord or peripheral nerves. Several Suppressor of Cytokine Signaling (SOCS) proteins have been shown to limit pro-inflammatory signaling pathways in myeloid cells and prevent neuroinflammation. They rely on several mechanisms to accomplish this. Their SH2 domain allows them to bind phosphorylated tyrosine residues on surface receptors to prevent downstream signaling while their C-terminal SOCS domain can promote their assembly with Cullin5 (CUL5) to degrade signaling proteins. To date, the role of CUL5 in myeloid-cell-mediated function is poorly understood. Here we show that loss of Cul5 in myeloid cells resulted in reduced neuroinflammation and attenuated progression of Experimental Autoimmune Encephalomyelitis (EAE). Although peripheral CD4+ T cell activation was not overtly affected, Cul5-deficient macrophages in the Central Nervous System (CNS) demonstrated a significant shift toward an anti-inflammatory phenotype, characterized by increased expression of Arginase 1. This correlated with an enhanced frequency of FoxP3+ regulatory T cells. In contrast to what would be predicted if CUL5 and SOCS proteins work together to degrade pro-inflammatory cytokine signaling, Cul5 deletion in myeloid cells selectively enhanced IL-4-mediated Arginase 1 expression. These findings identify CUL5 as an unanticipated pro-inflammatory mediator during neuroinflammation and reveal its potential as a therapeutic target for autoimmune diseases.
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spelling doaj-art-e87044095edd48bb8eadc4c8e9565e0c2025-08-20T03:44:43ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-08-011610.3389/fimmu.2025.16118181611818Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammationYohaniz Ortega-Burgos0Yohaniz Ortega-Burgos1Asif A. Dar2Siera A. Tomishima3Siera A. Tomishima4Ipsita Guha5Carleigh O’ Brien6Nadia Porter7F. Chris Bennett8F. Chris Bennett9Paula M. Oliver10Paula M. Oliver11Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDivision of Protective Immunity, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDivision of Protective Immunity, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDivision of Protective Immunity, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDivision of Protective Immunity, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDivision of Neurology, Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDivision of Protective Immunity, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesAutoimmune neuroinflammation occurs when an individual’s immune cells attack the brain, spinal cord or peripheral nerves. Several Suppressor of Cytokine Signaling (SOCS) proteins have been shown to limit pro-inflammatory signaling pathways in myeloid cells and prevent neuroinflammation. They rely on several mechanisms to accomplish this. Their SH2 domain allows them to bind phosphorylated tyrosine residues on surface receptors to prevent downstream signaling while their C-terminal SOCS domain can promote their assembly with Cullin5 (CUL5) to degrade signaling proteins. To date, the role of CUL5 in myeloid-cell-mediated function is poorly understood. Here we show that loss of Cul5 in myeloid cells resulted in reduced neuroinflammation and attenuated progression of Experimental Autoimmune Encephalomyelitis (EAE). Although peripheral CD4+ T cell activation was not overtly affected, Cul5-deficient macrophages in the Central Nervous System (CNS) demonstrated a significant shift toward an anti-inflammatory phenotype, characterized by increased expression of Arginase 1. This correlated with an enhanced frequency of FoxP3+ regulatory T cells. In contrast to what would be predicted if CUL5 and SOCS proteins work together to degrade pro-inflammatory cytokine signaling, Cul5 deletion in myeloid cells selectively enhanced IL-4-mediated Arginase 1 expression. These findings identify CUL5 as an unanticipated pro-inflammatory mediator during neuroinflammation and reveal its potential as a therapeutic target for autoimmune diseases.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1611818/fullCullin 5neuroinflammationmacrophagesubiquitin ligase (E3)macrophage polarization
spellingShingle Yohaniz Ortega-Burgos
Yohaniz Ortega-Burgos
Asif A. Dar
Siera A. Tomishima
Siera A. Tomishima
Ipsita Guha
Carleigh O’ Brien
Nadia Porter
F. Chris Bennett
F. Chris Bennett
Paula M. Oliver
Paula M. Oliver
Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
Frontiers in Immunology
Cullin 5
neuroinflammation
macrophages
ubiquitin ligase (E3)
macrophage polarization
title Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
title_full Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
title_fullStr Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
title_full_unstemmed Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
title_short Loss of Cullin 5 in myeloid cells protects against autoimmune neuroinflammation
title_sort loss of cullin 5 in myeloid cells protects against autoimmune neuroinflammation
topic Cullin 5
neuroinflammation
macrophages
ubiquitin ligase (E3)
macrophage polarization
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1611818/full
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