Modeling of TREX1-Dependent Autoimmune Disease using Human Stem Cells Highlights L1 Accumulation as a Source of Neuroinflammation

Cell Stem Cell. 2017 Sep 7;21(3):319-331.e8. doi: 10.1016/j.stem.2017.07.009. Epub 2017 Aug 10.

Abstract

Three-prime repair exonuclease 1 (TREX1) is an anti-viral enzyme that cleaves nucleic acids in the cytosol, preventing accumulation and a subsequent type I interferon-associated inflammatory response. Autoimmune diseases, including Aicardi-Goutières syndrome (AGS) and systemic lupus erythematosus, can arise when TREX1 function is compromised. AGS is a neuroinflammatory disorder with severe and persistent intellectual and physical problems. Here we generated a human AGS model that recapitulates disease-relevant phenotypes using pluripotent stem cells lacking TREX1. We observed abundant extrachromosomal DNA in TREX1-deficient neural cells, of which endogenous Long Interspersed Element-1 retrotransposons were a major source. TREX1-deficient neurons also exhibited increased apoptosis and formed three-dimensional cortical organoids of reduced size. TREX1-deficient astrocytes further contributed to the observed neurotoxicity through increased type I interferon secretion. In this model, reverse-transcriptase inhibitors rescued the neurotoxicity of AGS neurons and organoids, highlighting their potential utility in therapeutic regimens for AGS and related disorders.

Keywords: Aicardi-Goutières syndrome; LINE-1; TREX1; disease modeling; neuroinflammation; type I IFN.

Publication types

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

MeSH terms

  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Autoimmune Diseases / enzymology*
  • Base Sequence
  • Cell Extracts
  • Child
  • Cytosol / metabolism
  • DNA / metabolism
  • Exodeoxyribonucleases / deficiency
  • Exodeoxyribonucleases / genetics
  • Exodeoxyribonucleases / metabolism*
  • Humans
  • Infant
  • Infant, Newborn
  • Inflammation / pathology*
  • Interferons / pharmacology
  • Long Interspersed Nucleotide Elements / genetics*
  • Male
  • Microcephaly / pathology
  • Nervous System / pathology*
  • Neural Stem Cells / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Organoids / metabolism
  • Phenotype
  • Phosphoproteins / deficiency
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Stem Cells / drug effects
  • Stem Cells / metabolism*
  • Up-Regulation / drug effects
  • Up-Regulation / genetics

Substances

  • Cell Extracts
  • Phosphoproteins
  • DNA
  • Interferons
  • Exodeoxyribonucleases
  • three prime repair exonuclease 1