T Cells Produce IFN-α in the TREX1 D18N Model of Lupus-like Autoimmunity

J Immunol. 2020 Jan 15;204(2):348-359. doi: 10.4049/jimmunol.1900220. Epub 2019 Dec 11.

Abstract

Autoimmunity can result when cells fail to properly dispose of DNA. Mutations in the three-prime repair exonuclease 1 (TREX1) cause a spectrum of human autoimmune diseases resembling systemic lupus erythematosus. The cytosolic dsDNA sensor, cyclic GMP-AMP synthase (cGAS), and the stimulator of IFN genes (STING) are required for pathogenesis, but specific cells in which DNA sensing and subsequent type I IFN (IFN-I) production occur remain elusive. In this study, we demonstrate that TREX1 D18N catalytic deficiency causes dysregulated IFN-I signaling and autoimmunity in mice. Moreover, we show that bone marrow-derived cells drive this process. We identify both innate immune and, surprisingly, activated T cells as sources of pathological IFN-α production. These findings demonstrate that TREX1 enzymatic activity is crucial to prevent inappropriate DNA sensing and IFN-I production in immune cells, including normally low-level IFN-α-producing cells. These results expand our understanding of DNA sensing and innate immunity in T cells and may have relevance to the pathogenesis of human disease caused by TREX1 mutation.

Publication types

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

MeSH terms

  • Animals
  • Autoantigens / immunology
  • Autoimmunity
  • Cells, Cultured
  • DNA / immunology
  • Disease Models, Animal
  • Exodeoxyribonucleases / genetics*
  • Humans
  • Immunity, Innate
  • Interferon-alpha / metabolism
  • Lupus Erythematosus, Systemic / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nucleotidyltransferases / metabolism
  • Phosphoproteins / genetics*
  • T-Lymphocytes / immunology*

Substances

  • Autoantigens
  • Interferon-alpha
  • Membrane Proteins
  • Phosphoproteins
  • Sting1 protein, mouse
  • DNA
  • Nucleotidyltransferases
  • cGAS protein, mouse
  • Exodeoxyribonucleases
  • three prime repair exonuclease 1