A conformational RNA zipper promotes intron ejection during non-conventional XBP1 mRNA splicing

EMBO Rep. 2015 Dec;16(12):1688-98. doi: 10.15252/embr.201540955. Epub 2015 Oct 19.

Abstract

The kinase/endonuclease IRE1 is the most conserved signal transducer of the unfolded protein response (UPR), an intracellular signaling network that monitors and regulates the protein folding capacity of the endoplasmic reticulum (ER). Upon sensing protein folding perturbations in the ER, IRE1 initiates the unconventional splicing of XBP1 mRNA culminating in the production of the transcription factor XBP1s, which expands the ER's protein folding capacity. We show that an RNA-intrinsic conformational change causes the intron of XBP1 mRNA to be ejected and the exons to zipper up into an extended stem, juxtaposing the RNA ends for ligation. These conformational rearrangements are important for XBP1 mRNA splicing in vivo. The features that point to such active participation of XBP1 mRNA in the splicing reaction are highly conserved throughout metazoan evolution, supporting their importance in orchestrating XBP1 mRNA processing with efficiency and fidelity.

Keywords: ER stress; RNA conformational change; XBP1 splicing; endoribonuclease; unfolded protein response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Conserved Sequence
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Endoplasmic Reticulum / genetics
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Humans
  • Introns*
  • Nucleic Acid Conformation
  • Protein Folding
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • RNA Splicing*
  • RNA, Messenger
  • Regulatory Factor X Transcription Factors
  • Sequence Alignment
  • Sequence Analysis, DNA
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Unfolded Protein Response
  • X-Box Binding Protein 1

Substances

  • DNA-Binding Proteins
  • RNA, Messenger
  • Regulatory Factor X Transcription Factors
  • Transcription Factors
  • X-Box Binding Protein 1
  • XBP1 protein, human
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases