Revealing molecular pathways for cancer cell fitness through a genetic screen of the cancer translatome

Cell Rep. 2021 Jun 29;35(13):109321. doi: 10.1016/j.celrep.2021.109321.

Abstract

The major cap-binding protein eukaryotic translation initiation factor 4E (eIF4E), an ancient protein required for translation of all eukaryotic genomes, is a surprising yet potent oncogenic driver. The genetic interactions that maintain the oncogenic activity of this key translation factor remain unknown. In this study, we carry out a genome-wide CRISPRi screen wherein we identify more than 600 genetic interactions that sustain eIF4E oncogenic activity. Our data show that eIF4E controls the translation of Tfeb, a key executer of the autophagy response. This autophagy survival response is triggered by mitochondrial proteotoxic stress, which allows cancer cell survival. Our screen also reveals a functional interaction between eIF4E and a single anti-apoptotic factor, Bcl-xL, in tumor growth. Furthermore, we show that eIF4E and the exon-junction complex (EJC), which is involved in many steps of RNA metabolism, interact to control the migratory properties of cancer cells. Overall, we uncover several cancer-specific vulnerabilities that provide further resolution of the cancer translatome.

Keywords: Bcl-xL; CRISPRi; EJC; Tfeb; UPR(mt)-like stress response; autophagy; cancer; eIF4E; mitochondria; translation control.

Publication types

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

MeSH terms

  • 5' Untranslated Regions / genetics
  • Animals
  • Apoptosis / genetics
  • Autophagy
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • CRISPR-Cas Systems / genetics
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Eukaryotic Initiation Factor-4E / genetics
  • Eukaryotic Initiation Factor-4E / metabolism
  • Exons / genetics
  • Genetic Testing*
  • Genome, Human
  • Humans
  • Male
  • Metalloendopeptidases / metabolism
  • Mice
  • Mitochondria / metabolism
  • Mitochondrial Proteins / metabolism
  • Neoplasms / genetics*
  • Neoplasms / pathology
  • Peptide Hydrolases / metabolism
  • Protein Biosynthesis* / genetics
  • Signal Transduction* / genetics
  • Stress, Physiological
  • bcl-X Protein / metabolism

Substances

  • 5' Untranslated Regions
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Eukaryotic Initiation Factor-4E
  • Mitochondrial Proteins
  • TFEB protein, human
  • bcl-X Protein
  • Peptide Hydrolases
  • Metalloendopeptidases
  • PMPCB protein, human