Divergent allosteric control of the IRE1α endoribonuclease using kinase inhibitors

Nat Chem Biol. 2012 Dec;8(12):982-9. doi: 10.1038/nchembio.1094. Epub 2012 Oct 21.

Abstract

Under endoplasmic reticulum stress, unfolded protein accumulation leads to activation of the endoplasmic reticulum transmembrane kinase/endoRNase (RNase) IRE1α. IRE1α oligomerizes, autophosphorylates and initiates splicing of XBP1 mRNA, thus triggering the unfolded protein response (UPR). Here we show that IRE1α's kinase-controlled RNase can be regulated in two distinct modes with kinase inhibitors: one class of ligands occupies IRE1α's kinase ATP-binding site to activate RNase-mediated XBP1 mRNA splicing even without upstream endoplasmic reticulum stress, whereas a second class can inhibit the RNase through the same ATP-binding site, even under endoplasmic reticulum stress. Thus, alternative kinase conformations stabilized by distinct classes of ATP-competitive inhibitors can cause allosteric switching of IRE1α's RNase--either on or off. As dysregulation of the UPR has been implicated in a variety of cell degenerative and neoplastic disorders, small-molecule control over IRE1α should advance efforts to understand the UPR's role in pathophysiology and to develop drugs for endoplasmic reticulum stress-related diseases.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Catalysis
  • Cells, Cultured
  • Cross-Linking Reagents
  • DNA-Binding Proteins / metabolism
  • Down-Regulation / drug effects
  • Endoplasmic Reticulum Stress / physiology
  • Endoribonucleases / antagonists & inhibitors*
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes / antagonists & inhibitors
  • Isoenzymes / metabolism
  • Molecular Conformation
  • Mutation / genetics
  • Mutation / physiology
  • Phosphorylation
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • RNA Splicing / drug effects
  • Regulatory Factor X Transcription Factors
  • Ribonucleases / metabolism
  • Transcription Factors / metabolism
  • Unfolded Protein Response / drug effects
  • Up-Regulation / drug effects
  • X-Box Binding Protein 1

Substances

  • Adaptor Proteins, Signal Transducing
  • CTNNBIP1 protein, human
  • Cross-Linking Reagents
  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes
  • Protein Kinase Inhibitors
  • Regulatory Factor X Transcription Factors
  • Transcription Factors
  • X-Box Binding Protein 1
  • XBP1 protein, human
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases
  • Ribonucleases

Associated data

  • PubChem-Substance/144203443
  • PubChem-Substance/144203444
  • PubChem-Substance/144203445
  • PubChem-Substance/144203446
  • PubChem-Substance/144203447
  • PubChem-Substance/144203448
  • PubChem-Substance/144203449
  • PubChem-Substance/144203450