Dual IRE1 RNase functions dictate glioblastoma development

EMBO Mol Med. 2018 Mar;10(3):e7929. doi: 10.15252/emmm.201707929.

Abstract

Proteostasis imbalance is emerging as a major hallmark of cancer, driving tumor aggressiveness. Evidence suggests that the endoplasmic reticulum (ER), a major site for protein folding and quality control, plays a critical role in cancer development. This concept is valid in glioblastoma multiform (GBM), the most lethal primary brain cancer with no effective treatment. We previously demonstrated that the ER stress sensor IRE1α (referred to as IRE1) contributes to GBM progression, through XBP1 mRNA splicing and regulated IRE1-dependent decay (RIDD) of RNA Here, we first demonstrated IRE1 signaling significance to human GBM and defined specific IRE1-dependent gene expression signatures that were confronted to human GBM transcriptomes. This approach allowed us to demonstrate the antagonistic roles of XBP1 mRNA splicing and RIDD on tumor outcomes, mainly through selective remodeling of the tumor stroma. This study provides the first demonstration of a dual role of IRE1 downstream signaling in cancer and opens a new therapeutic window to abrogate tumor progression.

Keywords: IRE1; XBP1; cancer; endoplasmic reticulum; regulated IRE1‐dependent decay.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain Neoplasms / enzymology*
  • Brain Neoplasms / genetics
  • Brain Neoplasms / pathology*
  • Carcinogenesis / genetics
  • Carcinogenesis / pathology*
  • Cell Line, Tumor
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism*
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma / enzymology*
  • Glioblastoma / genetics
  • Glioblastoma / pathology*
  • Humans
  • Models, Biological
  • Mutation / genetics
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Phenotype
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA Splicing / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction
  • Tumor Microenvironment / genetics

Substances

  • Neoplasm Proteins
  • RNA, Messenger
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases