SARS-CoV-2 propagation to the TPH2-positive neurons in the ventral tegmental area induces cell death via GSK3β-dependent accumulation of phosphorylated tau

PLoS One. 2024 Oct 30;19(10):e0312834. doi: 10.1371/journal.pone.0312834. eCollection 2024.

Abstract

COVID-19, an infectious disease caused by SARS-CoV-2, was declared a pandemic by the WHO in 2020. Psychiatric symptoms including sleep disturbance, memory impairment, and depression are associated with SARS-CoV-2 infection. These symptoms are causes long-term mental and physical distress in recovering patients; however, the underlying mechanism is unclear. In this study, we determined the effects of SARS-CoV-2 infection on brain tissue using k18hACE2 mice. Using brain tissue from 18hACE2 mice infected with SARS-CoV-2 through intranasal administration, SARS-CoV-2 spike protein and RNA were analyzed by immunohistochemical staining and in-situ hybridization. Immunohistochemical analysis revealed that Tryptophan hydroxylase 2 (TPH2)-positive cells and SARS-CoV-2 spike protein were co-localized in the ventral tegmental area of SARS-CoV-2-infected mice. We observed decreased TPH2 expression and increased accumulation of phosphorylated tau protein and Phospho-Histone H2A.X (γH2AX) expression in the ventral tegmental region. In addition, activation of glycogen synthase kinase 3β (GSK3β) was induced by SARS-CoV-2 infection. Overall, our results suggest that SARS-CoV-2 infection of TPH2-positive cells in the ventral tegmental area induces neuronal cell death through increased accumulation of phosphorylated tau. Attenuation of the GSK3β pathway and decreased serotonin synthesis through suppression of TPH2 expression may contribute to the development of neurological symptoms.

MeSH terms

  • Animals
  • COVID-19* / metabolism
  • COVID-19* / pathology
  • COVID-19* / virology
  • Cell Death
  • Glycogen Synthase Kinase 3 beta* / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Transgenic
  • Neurons* / metabolism
  • Neurons* / virology
  • Phosphorylation
  • SARS-CoV-2* / pathogenicity
  • SARS-CoV-2* / physiology
  • Spike Glycoprotein, Coronavirus / metabolism
  • Tryptophan Hydroxylase* / genetics
  • Tryptophan Hydroxylase* / metabolism
  • Ventral Tegmental Area* / metabolism
  • Ventral Tegmental Area* / virology
  • tau Proteins* / metabolism

Substances

  • tau Proteins
  • Glycogen Synthase Kinase 3 beta
  • Tryptophan Hydroxylase
  • Tph2 protein, mouse
  • Gsk3b protein, mouse
  • Spike Glycoprotein, Coronavirus
  • spike protein, SARS-CoV-2

Grants and funding

The author(s) received no specific funding for this work.