Cancer Cells Upregulate NRF2 Signaling to Adapt to Autophagy Inhibition

Dev Cell. 2019 Sep 23;50(6):690-703.e6. doi: 10.1016/j.devcel.2019.07.010. Epub 2019 Aug 1.

Abstract

While autophagy is thought to be an essential process in some cancer cells, it is unknown if or how such cancer cells can circumvent autophagy inhibition. To address this, we developed a CRISPR/Cas9 assay with dynamic live-cell imaging to measure acute effects of knockout (KO) of autophagy genes compared to known essential and non-essential genes. In some cancer cells, autophagy is as essential for cancer cell growth as mRNA transcription or translation or DNA replication. However, even these highly autophagy-dependent cancer cells evolve to circumvent loss of autophagy by upregulating NRF2, which is necessary and sufficient for autophagy-dependent cells to circumvent ATG7 KO and maintain protein homeostasis. Importantly, however, this adaptation increases susceptibly to proteasome inhibitors. These studies identify a common mechanism of acquired resistance to autophagy inhibition and show that selection to avoid tumor cell dependency on autophagy creates new, potentially actionable cancer cell susceptibilities.

Keywords: ATG7; CRISPR/Cas9; NRF2; autophagy; cancer; chloroquine resistance; oxidative stress; proteasomal degradation.

Publication types

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

MeSH terms

  • Adaptation, Physiological* / drug effects
  • Autophagy* / drug effects
  • Autophagy-Related Protein 7 / metabolism
  • CRISPR-Cas Systems / genetics
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Clone Cells
  • Gene Knockout Techniques
  • Genes, Essential
  • Humans
  • NF-E2-Related Factor 2 / metabolism*
  • Neoplasms / metabolism*
  • Neoplasms / pathology*
  • Proteasome Endopeptidase Complex / metabolism
  • Proteasome Inhibitors / pharmacology
  • Ribonucleoproteins / metabolism
  • Signal Transduction* / drug effects
  • Up-Regulation* / drug effects

Substances

  • NF-E2-Related Factor 2
  • Proteasome Inhibitors
  • Ribonucleoproteins
  • Proteasome Endopeptidase Complex
  • Autophagy-Related Protein 7