Interruption of post-Golgi STING trafficking activates tonic interferon signaling

Nat Commun. 2022 Nov 15;13(1):6977. doi: 10.1038/s41467-022-33765-0.

Abstract

Activation of the cGAS-STING pathway is traditionally considered a "trigger-release" mechanism where detection of microbial DNA or cyclic di-nucleotides sets off the type I interferon response. Whether this pathway can be activated without pathogenic ligand exposure is less well understood. Here we show that loss of Golgi-to-lysosome STING cofactors, but not ER-to-Golgi cofactors, selectively activates tonic interferon signalling. Impairment of post-Golgi trafficking extends STING Golgi-dwell time, resulting in elevated immune signalling and protection against infection. Mechanistically, trans-Golgi coiled coil protein GCC2 and several RAB GTPases act as key regulators of STING post-Golgi trafficking. Genomic deletion of these factors potently activates cGAS-STING signalling without instigating any pathogenic trigger for cGAS. Gcc2-/- mice develop STING-dependent serologic autoimmunity. Gcc2-deleted or Rab14-deleted cancer cells induce T-cell and IFN-dependent anti-tumour immunity and inhibit tumour growth in mice. In summary, we present a "basal flux" mechanism for tonic cGAS-STING signalling, regulated at the level of post-Golgi STING trafficking, which could be exploited for cancer immunotherapy.

Publication types

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

MeSH terms

  • Animals
  • Golgi Apparatus / metabolism
  • Immunity, Innate
  • Interferon Type I* / metabolism
  • Membrane Proteins* / metabolism
  • Mice
  • Nucleotides, Cyclic / metabolism
  • Nucleotidyltransferases / metabolism

Substances

  • Membrane Proteins
  • Nucleotidyltransferases
  • Nucleotides, Cyclic
  • Interferon Type I