Ceapins block the unfolded protein response sensor ATF6α by inducing a neomorphic inter-organelle tether

Elife. 2019 May 31:8:e46595. doi: 10.7554/eLife.46595.

Abstract

The unfolded protein response (UPR) detects and restores deficits in the endoplasmic reticulum (ER) protein folding capacity. Ceapins specifically inhibit the UPR sensor ATF6α, an ER-tethered transcription factor, by retaining it at the ER through an unknown mechanism. Our genome-wide CRISPR interference (CRISPRi) screen reveals that Ceapins function is completely dependent on the ABCD3 peroxisomal transporter. Proteomics studies establish that ABCD3 physically associates with ER-resident ATF6α in cells and in vitro in a Ceapin-dependent manner. Ceapins induce the neomorphic association of ER and peroxisomes by directly tethering the cytosolic domain of ATF6α to ABCD3's transmembrane regions without inhibiting or depending on ABCD3 transporter activity. Thus, our studies reveal that Ceapins function by chemical-induced misdirection which explains their remarkable specificity and opens up new mechanistic routes for drug development and synthetic biology.

Keywords: biochemistry; cell biology; chemical biology; human; proteostasis; small molecule inhibition; unfolded protein response.

Publication types

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

MeSH terms

  • ATP-Binding Cassette Transporters / metabolism
  • Activating Transcription Factor 6 / antagonists & inhibitors*
  • Activating Transcription Factor 6 / metabolism
  • CRISPR-Cas Systems / genetics
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / metabolism
  • HEK293 Cells
  • Hep G2 Cells
  • Humans
  • Organelles / drug effects
  • Organelles / metabolism*
  • Peroxisomes / drug effects
  • Peroxisomes / metabolism
  • Phenotype
  • Protein Binding / drug effects
  • Small Molecule Libraries / pharmacology*
  • Unfolded Protein Response* / drug effects

Substances

  • ABCD3 protein, human
  • ATP-Binding Cassette Transporters
  • Activating Transcription Factor 6
  • Small Molecule Libraries