Autophagy suppresses interleukin-1β (IL-1β) signaling by activation of p62 degradation via lysosomal and proteasomal pathways

J Biol Chem. 2012 Feb 3;287(6):4033-40. doi: 10.1074/jbc.M111.280065. Epub 2011 Dec 13.

Abstract

ATG16L1 is an essential component of the autophagasome. The T300A allele of ATG16L1 is associated with the increased susceptibility to Crohn disease. In this study, we identified a novel function of ATG16L1, which suppresses signaling of the pro-inflammatory cytokine IL-1β. Deletion of ATG16L1 in mouse embryonic fibroblasts significantly amplifies IL-1β signal transduction cascades. This amplification is due to elevated p62 levels in ATG16L1-deficient cells. We found that ATG16L1 regulates p62 levels via both autolysosomal and proteasomal pathways. For proteasomal degradation, we found that Cullin-3 (Cul-3) is a E3 ubiquitin ligase of p62 and that ATG16L1 is essential for neddylation of Cul-3, a step required for Cul-3 activation. Taken together our data indicate that loss-of-function of ATG16L1 results in a hyper-responsiveness to the IL-1β signaling because of the increased p62 level.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Autophagy / physiology*
  • Autophagy-Related Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Cullin Proteins / genetics
  • Cullin Proteins / metabolism
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / metabolism*
  • Enzyme Activation / physiology
  • Fibroblasts / cytology
  • Fibroblasts / metabolism*
  • Gene Deletion
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Mice
  • Mice, Knockout
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism
  • Sequestosome-1 Protein
  • Signal Transduction / physiology*

Substances

  • Adaptor Proteins, Signal Transducing
  • Atg16l1 protein, mouse
  • Autophagy-Related Proteins
  • Carrier Proteins
  • Cul3 protein, mouse
  • Cullin Proteins
  • Heat-Shock Proteins
  • Interleukin-1beta
  • Sequestosome-1 Protein
  • Sqstm1 protein, mouse
  • Proteasome Endopeptidase Complex