Repression of mRNA translation initiation by GIGYF1 via disrupting the eIF3-eIF4G1 interaction

Sci Adv. 2024 Jul 19;10(29):eadl5638. doi: 10.1126/sciadv.adl5638. Epub 2024 Jul 17.

Abstract

Viruses can selectively repress the translation of mRNAs involved in the antiviral response. RNA viruses exploit the Grb10-interacting GYF (glycine-tyrosine-phenylalanine) proteins 2 (GIGYF2) and eukaryotic translation initiation factor 4E (eIF4E) homologous protein 4EHP to selectively repress the translation of transcripts such as Ifnb1, which encodes the antiviral cytokine interferon-β (IFN-β). Herein, we reveal that GIGYF1, a paralog of GIGYF2, robustly represses cellular mRNA translation through a distinct 4EHP-independent mechanism. Upon recruitment to a target mRNA, GIGYF1 binds to subunits of eukaryotic translation initiation factor 3 (eIF3) at the eIF3-eIF4G1 interaction interface. This interaction disrupts the eIF3 binding to eIF4G1, resulting in transcript-specific translational repression. Depletion of GIGYF1 induces a robust immune response by derepressing IFN-β production. Our study highlights a unique mechanism of translational regulation by GIGYF1 that involves sequestering eIF3 and abrogating its binding to eIF4G1. This mechanism has profound implications for the host response to viral infections.

MeSH terms

  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Eukaryotic Initiation Factor-3* / genetics
  • Eukaryotic Initiation Factor-3* / metabolism
  • Eukaryotic Initiation Factor-4G* / genetics
  • Eukaryotic Initiation Factor-4G* / metabolism
  • Gene Expression Regulation
  • Humans
  • Interferon-beta / genetics
  • Interferon-beta / metabolism
  • Peptide Chain Initiation, Translational
  • Protein Binding*
  • Protein Biosynthesis
  • RNA, Messenger* / genetics
  • RNA, Messenger* / metabolism

Substances

  • Eukaryotic Initiation Factor-4G
  • Eukaryotic Initiation Factor-3
  • RNA, Messenger
  • EIF4G1 protein, human
  • Interferon-beta
  • Carrier Proteins
  • GIGYF2 protein, human