Acute frataxin knockdown in induced pluripotent stem cell-derived cardiomyocytes activates a type I interferon response

Dis Model Mech. 2023 May 1;16(5):dmm049497. doi: 10.1242/dmm.049497. Epub 2022 Oct 26.

Abstract

Friedreich ataxia, the most common hereditary ataxia, is a neuro- and cardio-degenerative disorder caused, in most cases, by decreased expression of the mitochondrial protein frataxin. Cardiomyopathy is the leading cause of premature death. Frataxin functions in the biogenesis of iron-sulfur clusters, which are prosthetic groups that are found in proteins involved in many biological processes. To study the changes associated with decreased frataxin in human cardiomyocytes, we developed a novel isogenic model by acutely knocking down frataxin, post-differentiation, in cardiomyocytes derived from induced pluripotent stem cells (iPSCs). Transcriptome analysis of four biological replicates identified severe mitochondrial dysfunction and a type I interferon response as the pathways most affected by frataxin knockdown. We confirmed that, in iPSC-derived cardiomyocytes, loss of frataxin leads to mitochondrial dysfunction. The type I interferon response was activated in multiple cell types following acute frataxin knockdown and was caused, at least in part, by release of mitochondrial DNA into the cytosol, activating the cGAS-STING sensor pathway.

Keywords: Cardiomyopathy; Friedreich ataxia; Innate immunity; Interferon; mtDNA.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • DNA, Mitochondrial / metabolism
  • Frataxin
  • Friedreich Ataxia* / genetics
  • Friedreich Ataxia* / metabolism
  • Humans
  • Induced Pluripotent Stem Cells* / metabolism
  • Interferon Type I* / metabolism
  • Iron / metabolism
  • Iron-Binding Proteins / genetics
  • Iron-Binding Proteins / metabolism
  • Mitochondrial Proteins / metabolism
  • Myocytes, Cardiac / metabolism
  • Nucleotidyltransferases / metabolism
  • Sulfur / metabolism

Substances

  • Interferon Type I
  • Iron-Binding Proteins
  • Mitochondrial Proteins
  • Iron
  • DNA, Mitochondrial
  • Nucleotidyltransferases
  • Sulfur