Interferon-γ Potentiates α-Synuclein-induced Neurotoxicity Linked to Toll-like Receptors 2 and 3 and Tumor Necrosis Factor-α in Murine Astrocytes

Mol Neurobiol. 2019 Nov;56(11):7664-7679. doi: 10.1007/s12035-019-1567-5. Epub 2019 May 16.

Abstract

α-Synuclein (α-syn), a metabolite of neurons, induces glial activation and neuroinflammation and participates in pathogenesis of neurodegenerative diseases. This inflammatory response involves activation of toll-like receptors (TLRs) and its neurotoxic outcomes such as cytokine expression and release. However, regulatory role of cytokines on α-syn-induced neurotoxicity is still unclear. In this study, we used interferon (IFN)-γ to costimulate primary astrocytes with wild-type or A53T mutant α-syn, and evaluated inflammatory pathway activation. Four α-syn concentrations (0.5, 2, 8 and 20 μg/mL, 24 h) and four α-syn time-points (3, 12, 24 and 48 h, 2 μg/mL) were chosen to coincubate with one IFN-γ concentration (2 ng/mL). IFN-γ alone upregulated expressions of TLR3 and tumor necrosis factor (TNF)-α (mRNA level), and A53T mutant or wild-type α-syn alone activated the pathway components including TLR2, TLR3, nuclear factor-κB, TNF-α and interleukin (IL)-1β. Additive application of IFN-γ amplified this activation effect except for IL-1β at mRNA and protein levels or TNF-α release, displaying a synergistic effect of α-syn and IFN-γ. Blocking TLR2 other than TLR4 suppressed TLR3, TLR2 and TNF-α expressions induced by α-syn or plus IFN-γ, reflecting an interaction of TLR2 and TLR3 in TNF-α expression. These data collectively showed that IFN-γ potentiated α-syn stimulation and inflammatory outcomes via TLR2, TLR3 and TNF-α other than IL-1β in astrocytes, suggesting that involvement of IFN-γ in α-syn-induced innate immunity may be required for initiation and maintenance of glial activation, a novel neurotoxic mechanism underlying pathogenesis of neurodegenerative diseases. Graphical Abstract IFN-γ potentiates α-synuclein (A53T or wild-type)-induced innate immunity, involving expressions of TLR2, TLR3, NF-κB, and TNF-α, other than IL-1β. This effect is suppressed by blockage of TLR2 other than TLR4, reflecting an interaction of TLR2 and TLR3 in TNF-α expression. Thus, involvement of IFN-γ in α-syn-induced neurotoxicity may be required for initiation and maintenance of glial activation, a novel neurotoxic mechanism underlying pathogenesis of neurodegenerative diseases.

Keywords: Astrocytes; Cytokines; Interferon-γ; Neuroinflammation; Toll-like receptors; α-Synuclein.

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Cells, Cultured
  • Female
  • Interferon-gamma / pharmacology*
  • Male
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism
  • Toll-Like Receptor 2 / metabolism*
  • Toll-Like Receptor 3 / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism*
  • alpha-Synuclein / toxicity*

Substances

  • NF-kappa B
  • Toll-Like Receptor 2
  • Toll-Like Receptor 3
  • Tumor Necrosis Factor-alpha
  • alpha-Synuclein
  • Interferon-gamma