Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes

Immunity. 2012 Dec 14;37(6):986-997. doi: 10.1016/j.immuni.2012.09.014. Epub 2012 Dec 6.

Abstract

Toll-like receptor-9 (TLR9) is largely responsible for discriminating self from pathogenic DNA. However, association of host DNA with autoantibodies activates TLR9, inducing the pathogenic secretion of type I interferons (IFNs) from plasmacytoid dendritic cells (pDCs). Here, we found that in response to DNA-containing immune complexes (DNA-IC), but not to soluble ligands, IFN-α production depended upon the convergence of the phagocytic and autophagic pathways, a process called microtubule-associated protein 1A/1B-light chain 3 (LC3)-associated phagocytosis (LAP). LAP was required for TLR9 trafficking into a specialized interferon signaling compartment by a mechanism that involved autophagy-related proteins, but not the conventional autophagic preinitiation complex, or adaptor protein-3 (AP-3). Our findings unveil a new role for nonconventional autophagy in inflammation and provide one mechanism by which anti-DNA autoantibodies, such as those found in several autoimmune disorders, bypass the controls that normally restrict the apportionment of pathogenic DNA and TLR9 to the interferon signaling compartment.

Publication types

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

MeSH terms

  • Animals
  • Antigen-Antibody Complex / immunology*
  • Autophagy / immunology*
  • DNA / immunology*
  • Humans
  • Immunoglobulin G / immunology
  • Interferon Type I / biosynthesis*
  • Membrane Transport Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Microtubule-Associated Proteins / metabolism
  • Phagocytosis / immunology
  • Phagosomes / metabolism
  • Protein Transport
  • Toll-Like Receptor 9 / immunology
  • Toll-Like Receptor 9 / metabolism

Substances

  • Antigen-Antibody Complex
  • Immunoglobulin G
  • Interferon Type I
  • Map1lc3b protein, mouse
  • Membrane Transport Proteins
  • Microtubule-Associated Proteins
  • Toll-Like Receptor 9
  • DNA