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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Peripheral administration of anti-miR155 in SOD1 mice reversed this abnormal phenotype of microglia and ameliorated the disease.
“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]
The Results report that peripheral anti-miR-155 improved performance and prolonged survival in SOD1 mice. But the same section explicitly says peripheral treatment had no effect on the pro-inflammatory microglial profile; it reversed the inflammatory profile of peripheral monocytes instead. (LLM, conf=0.90)
Experimental — accuracy not yet measuredLoss 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.
“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]
The Results section on the microglial signature reports loss of M0-associated genes alongside up-regulation of inflammatory genes in SOD1 mice. A separate Results section links stronger inflammatory-gene activation to greater disease severity in male than female SOD1 mice. The claim omits that the severity comparison is sex-specific and presents findings from one SOD1 model as applying to animal models more broadly; page numbers are unavailable in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredIn ALS mice, germ-line knock-out of miR-155 altered microglia polarization in vivo.
“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]
The Results section (page unavailable) reports that genetic deletion of miR-155 in SOD1G93A mice reduced pro-inflammatory gene expression in spinal microglia and restored M1 and M0 marker patterns in vivo. However, the Animals section says the knockout mice were produced by crossing B6-congenic SOD1G93A mice with miR-155-deficient mice; it does not identify the knockout cohort as B6/SJL-SOD1G93A mice. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn SOD1 mice (ALS model), increased miR-155 with downregulation of P2ry12, Tmem119, Olfml3, Egr1, Atf3, Jun, Fos, Mafb, Csf1r, Tgfb1, and Tgfbr1 results in suppressed phagocytosis.
“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]
The Results report increased miR-155, loss of the listed microglial genes, and impaired phagocytosis in SOD1 mice. They also report that deleting miR-155 restores phagocytic ability. The passages do not establish that downregulation of the listed genes caused the impaired phagocytosis, as the citing sentence implies; page numbers were not provided in our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measuredmiR-155 is upregulated in the spinal cords of end-stage ALS model SOD1G93A mice and human autopsy.
“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
The Discussion (page unavailable) says miR-155 was the most upregulated miRNA in microglia and spinal cord tissue of SOD1G93A mice and ALS subjects. The Results report increased miR-155 in human ALS spinal-cord specimens, and the Methods identify those specimens as post-mortem. The passages do not establish that the reported miR-155 increase in mice was specifically measured at end-stage. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Numerous studies targeting members of the TREM2/TYROBP pathway (Trem2, Tyrobp, and miR155) support beneficial outcomes associated with maintenance and/or restoration of homeostatic functions of microglia.
“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 <i>INPP5D</i> limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease (2023) · cites this paper as [55]
miR-155 upregulation was identified in human sporadic and familial amyotrophic lateral sclerosis.
“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]
Inhibiting miR-155 significantly delays disease progression in SOD1G93A mice.
“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
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 reciprocal regulation of both proteins in prion disease.
“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]
During many diseases, microglia lose their homeostatic molecular signature and functions, such as synaptic plasticity, and become chronically inflammatory.
“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]
In the SOD1 ALS mouse, Tau, presenilin 2, and ApoE pathways are activated in microglia, Apoe is among the most induced transcripts during progression, and loss of the homeostatic microglial signature occurs as early as 2 months before measurable disease onset.
“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]
Targeting miR-155 in microglia is beneficial in models of ALS.
“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]
In a mouse model and in human ALS, miR-155 has been validated as a target for therapy aimed at modulating microglia.
“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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A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
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Self-citationApoE4 markedly exacerbates tau-mediated neurodegeneration in a mouse model of tauopathy
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CNS inflammation and neurodegeneration
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Self-citationTREM2, microglia, and neurodegenerative diseases
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microRNA dysregulation in neurodegenerative diseases: A systematic review
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Dark microglia: A new phenotype predominantly associated with pathological states
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Self-citationTREM2 variants: new keys to decipher Alzheimer disease pathogenesis
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Microglia: Agents of the CNS Pro-Inflammatory Response
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Microglial Physiology and Pathophysiology: Insights from Genome-wide Transcriptional Profiling
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TREM2 deficiency impairs chemotaxis and microglial responses to neuronal injury
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Self-citationApoE facilitates the microglial response to amyloid plaque pathology
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Self-citationElucidating the Role of TREM2 in Alzheimer’s Disease
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Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury
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Microglia, Lifestyle Stress, and Neurodegeneration
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Self-citationThe identity and function of microglia in neurodegeneration
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ALS Genes in the Genomic Era and their Implications for FTD
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Single‐cell transcriptomics reveals distinct inflammation‐induced microglia signatures
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Microglia Versus Myeloid Cell Nomenclature during Brain Inflammation
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Switching of the Microglial Activation Phenotype Is a Possible Treatment for Depression Disorder
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The Kaleidoscope of Microglial Phenotypes
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Antisense oligonucleotides: translation from mouse models to human neurodegenerative diseases
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“Intraventricular delivery of ASOs against miR-155, a target miRNA found to be upregulated in ALS tissues, resulted in de-repression of miR-155 targets throughout the brain and spinal cord and remarkably led to a significant extension in survival of SOD1 mutant mice (Butovsky et al., 2015; Koval et al., 2013).”
MicroRNAs: Roles in Regulating Neuroinflammation
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Role of Microglia in Neurological Disorders and Their Potentials as a Therapeutic Target
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Self-citationmicroRNA-155 Regulates Alpha-Synuclein-Induced Inflammatory Responses in Models of Parkinson Disease
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MicroRNAs in epilepsy: pathophysiology and clinical utility
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Amyotrophic lateral sclerosis: translating genetic discoveries into therapies
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Glial Cells Shape Pathology and Repair After Spinal Cord Injury
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A20 critically controls microglia activation and inhibits inflammasome-dependent neuroinflammation
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The microglial ATP‐gated ion channel P2X7 as a CNS drug target
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Transcriptional control of microglia phenotypes in health and disease
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Microglia and Neuroinflammation: What Place for P2RY12?
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Functional roles and networks of non-coding RNAs in the pathogenesis of neurodegenerative diseases
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TDP-43 aggregation induced by oxidative stress causes global mitochondrial imbalance in ALS
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The role of microRNAs in neurodegenerative diseases: a review
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Characterization of Gene Expression Phenotype in Amyotrophic Lateral Sclerosis Monocytes
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MicroRNAs as regulators of brain function and targets for treatment of epilepsy
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Exosome-Based Delivery of miR-124 in a Huntington’s Disease Model
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Self-citationMiR-155: An Important Regulator of Neuroinflammation
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NurOwn, phase 2, randomized, clinical trial in patients with ALS
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Epigenetics Control Microglia Plasticity
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RNA metabolism in neurodegenerative disease
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MicroRNA-125b regulates microglia activation and motor neuron death in ALS
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Neuroinflammation: The central enabler of postoperative cognitive dysfunction
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Differential contribution of microglia and monocytes in neurodegenerative diseases
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Self-citationDifferential expression of miRNA 155 and miRNA 146a in Parkinson's disease patients
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Emerging Roles of miRNAs in Brain Development and Perinatal Brain Injury
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APOE genotype and sex affect microglial interactions with plaques in Alzheimer’s disease mice
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Do Microglial Sex Differences Contribute to Sex Differences in Neurodegenerative Diseases?
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In vivo inhibition of miR-155 significantly alters post-stroke inflammatory response
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Pro‐inflammatory activation of microglia in the brain of patients with sepsis
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Self-citationCentral nervous system myeloid cells as drug targets: current status and translational challenges
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miR-155 Deletion in Female Mice Prevents Diet-Induced Obesity
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New Insights into Oxidative Stress and Inflammatory Response in Neurodegenerative Diseases
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Dominant role of microglial and macrophage innate immune responses in human ischemic infarcts
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From the Cajal alumni Achúcarro and Río-Hortega to the rediscovery of never-resting microglia
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miR-155 Is Essential for Inflammation-Induced Hippocampal Neurogenic Dysfunction
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- 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 › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › 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
About these checks
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