Phosphorylation of IRE1 at S729 regulates RIDD in B cells and antibody production after immunization

J Cell Biol. 2018 May 7;217(5):1739-1755. doi: 10.1083/jcb.201709137. Epub 2018 Mar 6.

Abstract

To relieve endoplasmic reticulum (ER) stress, IRE1 splices XBP1 messenger RNA (mRNA) or engages regulated IRE1-dependent decay (RIDD) of other mRNAs. Upon XBP1 deficiency, IRE1 switches to perform RIDD. We examined IRE1 in XBP1-deficient B cells and discovered that IRE1 undergoes phosphorylation at S729. We generated an anti-phospho-S729 antibody to investigate such phosphorylation. Compared with pharmacological ER stress inducers or Toll-like receptor ligands, the bacterial subtilase cytotoxin has an unusual capability in causing rapid and strong phosphorylation at S729 and triggering B cells to express spliced XBP1. To assess the function of S729 in IRE1, we generated S729A knock-in mice and found S729 is critically important for lipopolysaccharide-stimulated plasmablasts to respond to additional ER stress and for antibody production in response to immunization. We further crossed mice carrying an S729A mutation or ΔIRE1 (missing the kinase domain) with B cell-specific XBP1-deficient mice to trigger RIDD and discovered a critical role for S729 in regulating RIDD in B cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antibody Formation*
  • B-Lymphocytes / metabolism*
  • Dithiothreitol / pharmacology
  • Endoplasmic Reticulum Stress / drug effects
  • Immunization*
  • Immunoglobulin G / blood
  • Immunoglobulin M / blood
  • Lipopolysaccharides
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism*
  • Mice, Inbred C57BL
  • Models, Animal
  • Models, Biological
  • Phosphorylation
  • Phosphoserine / metabolism*
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA Stability*
  • T-Lymphocytes / metabolism
  • Up-Regulation / drug effects
  • X-Box Binding Protein 1 / metabolism

Substances

  • Immunoglobulin G
  • Immunoglobulin M
  • Lipopolysaccharides
  • Membrane Proteins
  • X-Box Binding Protein 1
  • Xbp1 protein, mouse
  • Phosphoserine
  • Ern2 protein, mouse
  • Protein Serine-Threonine Kinases
  • Dithiothreitol