TDP-43 knockdown causes innate immune activation via protein kinase R in astrocytes

Neurobiol Dis. 2019 Dec:132:104514. doi: 10.1016/j.nbd.2019.104514. Epub 2019 Jun 21.

Abstract

TAR-DNA binding protein 43 (TDP-43) is a multifunctional RNA binding protein directly implicated in the etiology of amyotrophic lateral sclerosis (ALS). Previous studies have demonstrated that loss of TDP-43 function leads to intracellular accumulation of non-coding repetitive element transcripts and double-stranded RNA (dsRNA). These events could cause immune activation and contribute to the neuroinflammation observed in ALS, but this possibility has not been investigated. Here, we knock down TDP-43 in primary rat astrocytes via siRNA, and we use RNA-seq, immunofluorescence, and immunoblotting to show that this results in: 1) accumulation of repetitive element transcripts and dsRNA; and 2) pro-inflammatory gene and protein expression consistent with innate immune signaling and astrocyte activation. We also show that both chemical inhibition and siRNA knockdown of protein kinase R (PKR), a dsRNA-activated kinase implicated in the innate immune response, block the expression of all activation markers assayed. Based on these findings, we suggest that intracellular accumulation of endogenous dsRNA may be a novel and important mechanism underlying the pathogenesis of ALS (and perhaps other neurodegenerative diseases), and that PKR inhibitors may have the potential to prevent reactive astrocytosis in ALS.

Keywords: Amyotrophic lateral sclerosis; Protein kinase R; Reactive astrocytes; TDP-43.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / immunology*
  • Astrocytes / metabolism
  • Cell Survival / genetics
  • Cell Survival / immunology
  • Cells, Cultured
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / immunology*
  • Gene Knockdown Techniques / methods*
  • Immunity, Innate / genetics
  • Immunity, Innate / immunology*
  • Inflammation Mediators / immunology
  • Inflammation Mediators / metabolism
  • RNA, Double-Stranded / genetics
  • RNA, Double-Stranded / immunology
  • RNA, Double-Stranded / metabolism
  • RNA, Small Interfering / administration & dosage
  • RNA, Small Interfering / genetics
  • Rats

Substances

  • DNA-Binding Proteins
  • Inflammation Mediators
  • RNA, Double-Stranded
  • RNA, Small Interfering
  • Tardbp protein, rat