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Oligodendrocyte-specific Argonaute profiling identifies microRNAs associated with experimental autoimmune encephalomyelitis

Ma, Qin, Matsunaga, Atsuko, Ho, Brenda, Oksenberg, Jorge R., Didonna, Alessandro·2020·Journal of Neuroinflammation
DOI 10.1186/s12974-020-01964-5PMC PMC7552381
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Abstract

Background: MicroRNAs (miRNAs) belong to a class of evolutionary conserved, non-coding small RNAs with regulatory functions on gene expression. They negatively affect the expression of target genes by promoting either RNA degradation or translational inhibition. In recent years, converging studies have identified miRNAs as key regulators of oligodendrocyte (OL) functions. OLs are the cells responsible for the formation and maintenance of myelin in the central nervous system (CNS) and represent a principal target of the autoimmune injury in multiple sclerosis (MS). Methods: MiRAP is a novel cell-specific miRNA affinity-purification technique which relies on genetically tagging Argonaut 2 (AGO2), an enzyme involved in miRNA processing. Here, we exploited miRAP potentiality to characterize OL-specific miRNA dynamics in the MS model experimental autoimmune encephalomyelitis (EAE). Results: We show that 20 miRNAs are differentially regulated in OLs upon transition from pre-symptomatic EAE stages to disease peak. Subsequent in vitro differentiation experiments demonstrated that a sub-group of them affects the OL maturation process, mediating either protective or detrimental signals. Lastly, transcriptome profiling highlighted the endocytosis, ferroptosis, and FoxO cascades as the pathways associated with miRNAs mediating or inhibiting OL maturation. Conclusions: Altogether, our work supports a dual role for miRNAs in autoimmune demyelination. In particular, the enrichment in miRNAs mediating pro-myelinating signals suggests an active involvement of these non-coding RNAs in the homeostatic response toward neuroinflammatory injury.

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  • miR-6983 is downregulated in oligodendrocytes during experimental autoimmune encephalomyelitis (EAE), an animal model of demyelination, and is associated with disrupted ferroptosis pathways that are implicated in demyelination and neurodegeneration.

    “miR-6983 is downregulated in oligodendrocytes during experimental autoimmune encephalomyelitis (EAE), an animal model of demyelination, and is associated with disrupted ferroptosis pathways that are implicated in demyelination and neurodegeneration65.”

    From Mouse microglia express unique miRNA-mRNA networks to facilitate age-specific functions in the developing central nervous system (2023) · cites this paper as [65]

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Cited by

Sorted by citations

Authors
Ma, Q., Matsunaga, A., Ho, B., Oksenberg, J. R., & Didonna, A.
Venue
Journal of Neuroinflammation
Publisher
Springer Science and Business Media LLC
Published
2020-10-12
Volume
17
Issue
1
ISSN
1742-2094
DOI
10.1186/s12974-020-01964-5
PMC
PMC7552381
Cited by
15
References
5
Language
en
Licence
Funders
  • Fondazione Italiana Sclerosi Multipla (2014/B/1, 2017/B/3)
  • National Multiple Sclerosis Society (RG-1506-04510)

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