MiR-409-3p and MiR-1896 co-operatively participate in IL-17-induced inflammatory cytokine production in astrocytes and pathogenesis of EAE mice via targeting SOCS3/STAT3 signaling

Glia. 2019 Jan;67(1):101-112. doi: 10.1002/glia.23530. Epub 2018 Oct 7.

Abstract

Th17 cells and interleukin-17 (IL-17) have been found to play an important role in the pathology of multiple sclerosis (MS) and its animal model, experimental autoimmune encephalomyelitis (EAE). Response to IL-17, reactive astrocytes accompany with immune cells infiltration and axonal damage in MS/EAE. However, the role and the regulatory mechanism of IL-17-activated astrocytes in inflammation and in the EAE process still remain largely unknown. Here, we elucidated that miR-409-3p and miR-1896, as co-upregulated microRNAs in activated astrocytes and in EAE mice, targeted suppressor of cytokine signaling proteins 3 (SOCS3). Overexpression of miR-409-3p or miR-1896 significantly reduced SOCS3 expression and increased phosphorylation of STAT3 as well as induced the inflammatory cytokines production (IL-1β, IL-6, IP-10, MCP-1, and KC), CD4+ T cells migration and demyelination, in turn aggravating EAE development. Importantly, the effects of co-overexpression of miR-409-3p and miR-1896 in vitro or in vivo are strongly co-operative. In contrast, simultaneously silenced miR-409-3p and miR-1896 co-operatively ameliorates inflammation and demyelination in the central nervous system of EAE mice. Collectively, our findings highlight that miR-409-3p and miR-1896 co-ordinately promote the production of inflammatory cytokines in reactive astrocytes through the SOCS3/STAT3 pathway and enhance reactive astrocyte-directed chemotaxis of CD4+ T cells, leading to aggravate pathogenesis in EAE mice. Co-inhibition of miR-409-3p and miR-1896 may be a therapeutic target for treating MS and neuroinflammation.

Keywords: SOCS3; astrocytes; experimental autoimmune encephalomyelitis; inflammatory cytokines; microRNA; multiple sclerosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / immunology
  • Astrocytes / metabolism*
  • Cytokines / biosynthesis
  • Cytokines / immunology
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / metabolism*
  • Female
  • Inflammation / chemically induced
  • Inflammation / immunology
  • Inflammation / metabolism
  • Interleukin-17 / immunology
  • Interleukin-17 / toxicity*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / biosynthesis*
  • MicroRNAs / immunology
  • STAT3 Transcription Factor / immunology
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Suppressor of Cytokine Signaling 3 Protein / immunology
  • Suppressor of Cytokine Signaling 3 Protein / metabolism*

Substances

  • Cytokines
  • Il17a protein, mouse
  • Interleukin-17
  • MIRN1896 microRNA, mouse
  • MIRN409 microRNA, mouse
  • MicroRNAs
  • STAT3 Transcription Factor
  • Socs3 protein, mouse
  • Stat3 protein, mouse
  • Suppressor of Cytokine Signaling 3 Protein