Clathrin-associated AP-1 controls termination of STING signalling

Nature. 2022 Oct;610(7933):761-767. doi: 10.1038/s41586-022-05354-0. Epub 2022 Oct 19.

Abstract

Stimulator of interferon genes (STING) functions downstream of cyclic GMP-AMP synthase in DNA sensing or as a direct receptor for bacterial cyclic dinucleotides and small molecules to activate immunity during infection, cancer and immunotherapy1-10. Precise regulation of STING is essential to ensure balanced immune responses and prevent detrimental autoinflammation11-16. After activation, STING, a transmembrane protein, traffics from the endoplasmic reticulum to the Golgi, where its phosphorylation by the protein kinase TBK1 enables signal transduction17-20. The mechanism that ends STING signalling at the Golgi remains unknown. Here we show that adaptor protein complex 1 (AP-1) controls the termination of STING-dependent immune activation. We find that AP-1 sorts phosphorylated STING into clathrin-coated transport vesicles for delivery to the endolysosomal system, where STING is degraded21. We identify a highly conserved dileucine motif in the cytosolic C-terminal tail (CTT) of STING that, together with TBK1-dependent CTT phosphorylation, dictates the AP-1 engagement of STING. A cryo-electron microscopy structure of AP-1 in complex with phosphorylated STING explains the enhanced recognition of TBK1-activated STING. We show that suppression of AP-1 exacerbates STING-induced immune responses. Our results reveal a structural mechanism of negative regulation of STING and establish that the initiation of signalling is inextricably associated with its termination to enable transient activation of immunity.

Publication types

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

MeSH terms

  • Adaptor Protein Complex 1* / chemistry
  • Adaptor Protein Complex 1* / metabolism
  • Adaptor Protein Complex 1* / ultrastructure
  • Amino Acid Motifs
  • Clathrin* / metabolism
  • Cryoelectron Microscopy
  • DNA / metabolism
  • Endosomes / metabolism
  • Immunity, Innate
  • Lysosomes / metabolism
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism
  • Membrane Proteins / ultrastructure
  • Phosphorylation
  • Protein Serine-Threonine Kinases

Substances

  • Adaptor Protein Complex 1
  • Clathrin
  • DNA
  • Protein Serine-Threonine Kinases
  • Membrane Proteins