Noncanonical Fungal Autophagy Inhibits Inflammation in Response to IFN-γ via DAPK1

Cell Host Microbe. 2016 Dec 14;20(6):744-757. doi: 10.1016/j.chom.2016.10.012. Epub 2016 Nov 23.

Abstract

Defects in a form of noncanonical autophagy, known as LC3-associated phagocytosis (LAP), lead to increased inflammatory pathology during fungal infection. Although LAP contributes to fungal degradation, the molecular mechanisms underlying LAP-mediated modulation of inflammation are unknown. We describe a mechanism by which inflammation is regulated during LAP through the death-associated protein kinase 1 (DAPK1). The ATF6/C/EBP-β/DAPK1 axis activated by IFN-γ not only mediates LAP to Aspergillus fumigatus but also concomitantly inhibits Nod-like receptor protein 3 (NLRP3) activation and restrains pathogenic inflammation. In mouse models and patient samples of chronic granulomatous disease, which exhibit defective autophagy and increased inflammasome activity, IFN-γ restores reduced DAPK1 activity and dampens fungal growth. Additionally, in a cohort of hematopoietic stem cell-transplanted patients, a genetic DAPK1 deficiency is associated with increased inflammation and heightened aspergillosis susceptibility. Thus, DAPK1 is a potential drugable player in regulating the inflammatory response during fungal clearance initiated by IFN-γ.

MeSH terms

  • Animals
  • Aspergillosis / microbiology
  • Aspergillus fumigatus / metabolism
  • Autophagy / drug effects*
  • Autophagy / physiology*
  • Cell Line
  • Death-Associated Protein Kinases / drug effects
  • Death-Associated Protein Kinases / genetics
  • Death-Associated Protein Kinases / metabolism*
  • Fungi / metabolism*
  • Fungi / pathogenicity
  • Gene Expression Regulation, Fungal
  • Granulomatous Disease, Chronic / microbiology
  • Humans
  • Inflammation / metabolism*
  • Interferon-gamma / metabolism*
  • Interferon-gamma / pharmacology
  • Lung / pathology
  • Macrophages / drug effects
  • Macrophages / microbiology
  • Mice
  • Mice, Inbred C57BL
  • NLR Proteins / drug effects
  • Phagocytosis
  • Phagosomes
  • RAW 264.7 Cells / drug effects
  • RAW 264.7 Cells / microbiology
  • Spores, Fungal / metabolism

Substances

  • NLR Proteins
  • Interferon-gamma
  • DAPK1 protein, human
  • Dapk1 protein, mouse
  • Death-Associated Protein Kinases