The GCN2-ATF4 Signaling Pathway Induces 4E-BP to Bias Translation and Boost Antimicrobial Peptide Synthesis in Response to Bacterial Infection

Cell Rep. 2017 Nov 21;21(8):2039-2047. doi: 10.1016/j.celrep.2017.10.096.

Abstract

Bacterial infection often leads to suppression of mRNA translation, but hosts are nonetheless able to express immune response genes through as yet unknown mechanisms. Here, we use a Drosophila model to demonstrate that antimicrobial peptide (AMP) production during infection is paradoxically stimulated by the inhibitor of cap-dependent translation, 4E-BP (eIF4E-binding protein; encoded by the Thor gene). We found that 4E-BP is induced upon infection with pathogenic bacteria by the stress-response transcription factor ATF4 and its upstream kinase, GCN2. Loss of gcn2, atf4, or 4e-bp compromised immunity. While AMP transcription is unaffected in 4e-bp mutants, AMP protein levels are substantially reduced. The 5' UTRs of AMPs score positive in cap-independent translation assays, and this cap-independent activity is enhanced by 4E-BP. These results are corroborated in vivo using transgenic 5' UTR reporters. These observations indicate that ATF4-induced 4e-bp contributes to innate immunity by biasing mRNA translation toward cap-independent mechanisms, thus enhancing AMP synthesis.

Keywords: 4E-BP; 5'; ATF4; GCN2; UTR; antimicrobial peptides; innate immunity; internal ribosome entry site; mRNA translation.

MeSH terms

  • Activating Transcription Factor 4 / genetics*
  • Animals
  • Anti-Infective Agents / pharmacology*
  • Bacterial Infections / genetics
  • Carrier Proteins / metabolism
  • Drosophila
  • Drosophila Proteins / drug effects
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Eukaryotic Initiation Factor-4E / genetics
  • Intracellular Signaling Peptides and Proteins / drug effects
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Phosphorylation / physiology
  • Protein Binding / drug effects*
  • Protein Binding / genetics
  • Protein Biosynthesis / physiology
  • Protein Kinases / drug effects
  • Protein Kinases / metabolism*
  • Signal Transduction / drug effects

Substances

  • Anti-Infective Agents
  • Carrier Proteins
  • Drosophila Proteins
  • Eukaryotic Initiation Factor-4E
  • Intracellular Signaling Peptides and Proteins
  • cup protein, Drosophila
  • Activating Transcription Factor 4
  • GCN2 protein, Drosophila
  • Protein Kinases