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Targeting mi R‐155 restores abnormal microglia and attenuates disease in SOD 1 mice
Open accessAbstract
Objective: To investigate miR‐155 in the SOD1 mouse model and human sporadic and familial amyotrophic lateral sclerosis (ALS). Methods: NanoString microRNA, microglia and immune gene profiles, protein mass spectrometry, and RNA‐seq analyses were measured in spinal cord microglia, splenic monocytes, and spinal cord tissue from SOD1 mice and in spinal cord tissue of familial and sporadic ALS. miR‐155 was targeted by genetic ablation or by peripheral or centrally administered anti–miR‐155 inhibitor in SOD1 mice. Results: In SOD1 mice, we found loss of the molecular signature that characterizes homeostatic microglia and increased expression of miR‐155. There was loss of the microglial molecules P2ry12, Tmem119, Olfml3, transcription factors Egr1, Atf3, Jun, Fos, and Mafb, and the upstream regulators Csf1r, Tgfb1, and Tgfbr1, which are essential for microglial survival. Microglia biological functions were suppressed including phagocytosis. Genetic ablation of miR‐155 increased survival in SOD1 mice by 51 days in females and 27 days in males and restored the abnormal microglia and monocyte molecular signatures. Disease severity in SOD1 males was associated with early upregulation of inflammatory genes, including Apoe in microglia. Treatment of adult microglia with apolipoprotein E suppressed the M0‐homeostatic unique microglia signature and induced an M1‐like phenotype. miR‐155 expression was increased in the spinal cord of both familial and sporadic ALS. Dysregulated proteins that we identified in human ALS spinal cord were restored in SOD1 G93A/miR‐155−/− mice. Intraventricular anti–miR‐155 treatment derepressed microglial miR‐155 targeted genes, and peripheral anti–miR‐155 treatment prolonged survival. Interpretation: We found overexpression of miR‐155 in the SOD1 mouse and in both sporadic and familial human ALS. Targeting miR‐155 in SOD1 mice restores dysfunctional microglia and ameliorates disease. These findings identify miR‐155 as a therapeutic target for the treatment of ALS. ANN NEUROL 2015;77:75–99
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“It has been reported that peripheral administration of anti-miR155 in SOD1 mice reversed this abnormal phenotype of microglia and ameliorated the disease [6].”
From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [6]
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“Loss of the M0-homeostatic microglial signature in animal models of amyotrophic lateral sclerosis (ALS) is associated with up-regulation of inflammatory genes, which correlates with disease severity [6].”
From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [6]
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“In ALS (B6/SJL-SOD1G93A transgenic) mice it has been shown that germ-line knock-out of miR-155 altered microglia polarization in vivo [46].”
From Microglia specific deletion of miR-155 in Alzheimer’s disease mouse models reduces amyloid-β pathology but causes hyperexcitability and seizures (2023) · cites this paper as [46]
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“Increased expression of miR-155, with concomitant downregulation of numerous genes, namely P2ry12, Tmem119, Olfml3, Egr1, Atf3, Jun, Fos, Mafb, Csf1r, Tgfb1 and Tgfbr1, which resulted in suppressed phagocytosis, was also found in SOD1 mice, a murine model of amyotrophic lateral sclerosis.”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [238]
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“Work from our lab and others found that miR-155, a glialenriched miRNA, is upregulated in the spinal cords of end-stage ALS model (SOD1 G93A ) mice and human autopsy (Koval et al., 2013;Butovsky et al., 2015).”
From MicroRNA Profiling Reveals Marker of Motor Neuron Disease in ALS Models (2017) · cites this paper as Butovsky et al., 2015
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“In the context of CNS damage resulting from Aβ, tau, SOD-1, or other pathologies, apoE is strongly upregulated in microglia coincident with the DAM or MGnD phenotype (Butovsky et al., 2015; Keren-Shaul et al., 2017; Krasemann et al., 2017; Parhizkar et al., 2019; Shi et al., 2017).”
From Selective removal of astrocytic APOE4 strongly protects against tau-mediated neurodegeneration and decreases synaptic phagocytosis by microglia (2021) · cites this paper as Butovsky et al., 2015
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“miRNAs are increasingly recognized as key regulators in ALS pathophysiology, including mitochondrial integrity and neuroinflammation, with miR-155 and miR-206 demonstrating pivotal roles in SOD1G93A models [48,49,50,51].”
From Modulation of the miR-485-3p/PGC-1α Pathway by ASO-Loaded Nanoparticles Attenuates ALS Pathogenesis (2026) · cites this paper as [49]
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“Support for beneficial outcomes associated with maintenance and/or restoration of homeostatic functions of microglia comes from the numerous studies targeting the members of this pathway, including Trem2,48,50–52 Tyrobp,53,54 and miR155.41,55”
From Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease (2023) · cites this paper as [55]
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“As upregulation of miR-155 was also identified in human sporadic and familial amyotrophic lateral sclerosis”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [238]
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“Inhibiting miR-155 significantly delays disease progression in SOD1 G93A mice (Koval et al., 2013;Butovsky et al., 2015).”
From MicroRNA Profiling Reveals Marker of Motor Neuron Disease in ALS Models (2017) · cites this paper as Butovsky et al., 2015
In the citing paper
“The loss of homeostatic microglial proteins is visible in immunofluorescence double-staining of IBA1 and TMEM119 in terminally sick mice and mock-infected healthy control brains, and shows the reciprocal regulation of both proteins in prion disease (Figure 5A) [55,73,88,89,90,91].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [89]
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“during the course of many diseases, microglia lose their homeostatic molecular signature and functions26,84,114, such as their roles in synaptic plasticity115, and become chronically inflammatory116.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [84]
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“Tau, presenilin 2 and apolipoprotein E (ApoE) pathways were found to be activated in microglia in the SOD1 mouse, with Apoe being one of the transcripts that was the most significantly induced during disease progression.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [84]
In the citing paper
“Targeting miR-155 in microglia has shown to be a benefit in models of ALS84,195 and is currently being pursued as a possible therapeutic strategy.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [84]
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“This study validates miR-155 as a therapeutic target to modulate microglia in a mouse model and in human ALS.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [84]
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Metadata
- Authors
- Butovsky, O., Jedrychowski, M. P., Cialic, R., Krasemann, S., Murugaiyan, G., Fanek, Z., Greco, D. J., Wu, P. M., Doykan, C. E., Kiner, O., Lawson, R. J., Frosch, M. P., Pochet, N., Fatimy, R. E., Krichevsky, A. M., Gygi, S. P., Lassmann, H., Berry, J., Cudkowicz, M. E., & Weiner, H. L.
- Affiliations
- Brigham and Women's Hospital (US)
- Harvard University (US)
- University Medical Center Hamburg-Eppendorf (DE)
- Broad Institute (US)
- Medical University of Vienna (AT)
- Corresponding author
- Butovsky, Oleg
- ORCID
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2014-11-27
- Volume
- 77
- Issue
- 1
- Pages
- 75-99
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- PMC
- PMC4432483
- OpenAlex
- W1545421865
- Cited by
- 358
- References
- 63
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 33 · 2023: 31 · 2022: 46 · 2021: 32 · 2020: 33 · 2019: 29 · 2018: 41 · 2017: 35 · 2016: 26 · 2015: 20
- FWCI
- 17.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (NS088137)
- U.S. Department of Defense (AL120029)
- Amyotrophic Lateral Sclerosis Association (IV78RI, ALSA2087)
- National Multiple Sclerosis Society
- The Nancy Davis Foundation for Multiple Sclerosis
- Edward N. & Della L. Thome Memorial Foundation
- Topics
- Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Keywords
- miR-155, amyotrophic lateral sclerosis, microglia, microglial homeostasis, apolipoprotein E, microglial phagocytosis, microglial survival, therapeutic target, familial ALS, sporadic ALS
- MeSH terms
- Aged, Amyotrophic Lateral Sclerosis, Animals, Apolipoproteins E, Cells, Cultured, Disease Models, Animal, Female, Gene Expression Regulation, Hippocampus, Humans, Male, Mice, Transgenic, Middle Aged, Monocytes, Neurons, Phagocytosis, Spinal Cord, Superoxide Dismutase, Transforming Growth Factor beta, Microglia, Oligoribonucleotides, Antisense, MicroRNAs, Mice
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