Innate immune signaling in Drosophila is regulated by transforming growth factor β (TGFβ)-activated kinase (Tak1)-triggered ubiquitin editing

J Biol Chem. 2017 May 26;292(21):8738-8749. doi: 10.1074/jbc.M117.788158. Epub 2017 Apr 4.

Abstract

Coordinated regulation of innate immune responses is necessary in all metazoans. In Drosophila the Imd pathway detects Gram-negative bacterial infections through recognition of diaminopimelic acid (DAP)-type peptidoglycan and activation of the NF-κB precursor Relish, which drives robust antimicrobial peptide gene expression. Imd is a receptor-proximal adaptor protein homologous to mammalian RIP1 that is regulated by proteolytic cleavage and Lys-63-polyubiquitination. However, the precise events and molecular mechanisms that control the post-translational modification of Imd remain unclear. Here, we demonstrate that Imd is rapidly Lys-63-polyubiquitinated at lysine residues 137 and 153 by the sequential action of two E2 enzymes, Ubc5 and Ubc13-Uev1a, in conjunction with the E3 ligase Diap2. Lys-63-ubiquitination activates the TGFβ-activated kinase (Tak1), which feeds back to phosphorylate Imd, triggering the removal of Lys-63 chains and the addition of Lys-48 polyubiquitin. This ubiquitin-editing process results in the proteasomal degradation of Imd, which we propose functions to restore homeostasis to the Drosophila immune response.

Keywords: Drosophila; Imd; NF-κB (NF-κB); Tak1; antimicrobial peptide (AMP); mass spectrometry (MS); phosphorylation; ubiquitin editing; ubiquitylation (ubiquitination).

MeSH terms

  • Animals
  • Drosophila Proteins / genetics
  • Drosophila Proteins / immunology*
  • Drosophila melanogaster
  • Immunity, Innate*
  • Inhibitor of Apoptosis Proteins / genetics
  • Inhibitor of Apoptosis Proteins / immunology
  • MAP Kinase Kinase Kinases / genetics
  • MAP Kinase Kinase Kinases / immunology*
  • Polyubiquitin / genetics
  • Polyubiquitin / immunology
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Transcription Factors / genetics
  • Transcription Factors / immunology
  • Ubiquitin-Conjugating Enzymes / genetics
  • Ubiquitin-Conjugating Enzymes / immunology
  • Ubiquitination / genetics
  • Ubiquitination / immunology*

Substances

  • DIAP2 protein, Drosophila
  • Drosophila Proteins
  • Inhibitor of Apoptosis Proteins
  • Rel protein, Drosophila
  • Transcription Factors
  • imd protein, Drosophila
  • Polyubiquitin
  • Ubiquitin-Conjugating Enzymes
  • Uev1a protein, Drosophila
  • MAP Kinase Kinase Kinases
  • TAK1 protein, Drosophila