Single-cell RNA-sequencing analysis reveals α-syn induced astrocyte-neuron crosstalk-mediated neurotoxicity

Int Immunopharmacol. 2024 Sep 30:139:112676. doi: 10.1016/j.intimp.2024.112676. Epub 2024 Jul 24.

Abstract

Accumulation of alpha-synuclein (α-syn) is a key pathological hallmark of synucleinopathies and has been shown to negatively impact neuronal function and activity. α-syn is an important factor contributing to astrocyte overactivation, though the effect of astrocyte overactivation on neurons remains unclear. Single-cell RNA sequencing data of mouse brain frontal cortex and midbrain from Hua-Syn (A53T) and wild type mice were utilized from the GEO database. Enrichment analysis, protein-protein interaction networks, and cell-cell interaction networks all indicated enhanced communication between astrocytes and neurons, along with the involvement of TNF and inflammation-related signaling pathways. In vitro experiments were performed to further explore the mechanism of neurotoxicity in astrocyte-neuron crosstalk. Astrocytes were treated by α-syn, neuronal TNFR1 receptors were antagonized by R-7050, and the cells were co-cultured after 24 h treatment. ELISA results revealed that cytokines such as TNF-α and IL-6 were significantly upregulated in astrocytes following the endocytosis of α-syn. Immunofluorescence (IF) showed neuronal dendritic reduction, axon elongation and increased co-localisation of TNFR1 receptor expression. Western blot showed up-regulation of PKR, P-eIF2α and ATF4 protein expression. Conversely, after antagonizing neuronal TNFR1 receptors with the R-7050 chemical inhibitor, neuronal synaptic structure was significantly restored and the expression of PKR, P-eIF2α and ATF4 was down-regulated. In summary, TNF-α acts as a signaling molecule mediating the up-regulated astrocyte-neuron crosstalk, providing new insights into the pathogenesis of α-syn-related neurological disorders.

Keywords: Astrocyte; Neuron; TNF-α; scRNA-seq; α-synuclein.

MeSH terms

  • Animals
  • Astrocytes* / drug effects
  • Astrocytes* / metabolism
  • Cell Communication*
  • Cells, Cultured
  • Coculture Techniques
  • Mice
  • Mice, Transgenic
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Receptors, Tumor Necrosis Factor, Type I* / genetics
  • Receptors, Tumor Necrosis Factor, Type I* / metabolism
  • Sequence Analysis, RNA
  • Signal Transduction
  • Single-Cell Analysis*
  • Tumor Necrosis Factor-alpha / metabolism
  • alpha-Synuclein* / genetics
  • alpha-Synuclein* / metabolism

Substances

  • Receptors, Tumor Necrosis Factor, Type I
  • alpha-Synuclein
  • Tumor Necrosis Factor-alpha
  • Tnfrsf1a protein, mouse