Targeted ASO-mediated Atp1a2 knockdown in astrocytes reduces SOD1 aggregation and accelerates disease onset in mutant SOD1 mice

PLoS One. 2023 Nov 28;18(11):e0294731. doi: 10.1371/journal.pone.0294731. eCollection 2023.

Abstract

Astrocyte-specific ion pump α2-Na+/K+-ATPase plays a critical role in the pathogenesis of amyotrophic lateral sclerosis (ALS). Here, we test the effect of Atp1a2 mRNA-specific antisense oligonucleotides (ASOs) to induce α2-Na+/K+-ATPase knockdown in the widely used ALS animal model, SOD1*G93A mice. Two ASOs led to efficient Atp1a2 knockdown and significantly reduced SOD1 aggregation in vivo. Although Atp1a2 ASO-treated mice displayed no off-target or systemic toxicity, the ASO-treated mice exhibited an accelerated disease onset and shorter lifespan than control mice. Transcriptomics studies reveal downregulation of genes involved in oxidative response, metabolic pathways, trans-synaptic signaling, and upregulation of genes involved in glutamate receptor signaling and complement activation, suggesting a potential role for these molecular pathways in de-coupling SOD1 aggregation from survival in Atp1a2 ASO-treated mice. Together, these results reveal a role for α2-Na+/K+-ATPase in SOD1 aggregation and highlight the critical effect of temporal modulation of genetically validated therapeutic targets in neurodegenerative diseases.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / pathology
  • Animals
  • Astrocytes / metabolism
  • Disease Models, Animal
  • Mice
  • Mice, Transgenic
  • Motor Neurons / metabolism
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Spinal Cord / metabolism
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1 / genetics
  • Superoxide Dismutase-1 / metabolism

Substances

  • Atp1a2 protein, mouse
  • Sodium-Potassium-Exchanging ATPase
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Sod1 protein, mouse