A short isoform of STIM1 confers frequency-dependent synaptic enhancement

Cell Rep. 2021 Mar 16;34(11):108844. doi: 10.1016/j.celrep.2021.108844.

Abstract

Store-operated Ca2+-entry (SOCE) regulates basal and receptor-triggered Ca2+ signaling with STIM proteins sensing the endoplasmic reticulum (ER) Ca2+ content and triggering Ca2+ entry by gating Orai channels. Although crucial for immune cells, STIM1's role in neuronal Ca2+ homeostasis is controversial. Here, we characterize a splice variant, STIM1B, which shows exclusive neuronal expression and protein content surpassing conventional STIM1 in cerebellum and of significant abundance in other brain regions. STIM1B expression results in a truncated protein with slower kinetics of ER-plasma membrane (PM) cluster formation and ICRAC, as well as reduced inactivation. In primary wild-type neurons, STIM1B is targeted by its spliced-in domain B to presynaptic sites where it converts classic synaptic depression into Ca2+- and Orai-dependent short-term synaptic enhancement (STE) at high-frequency stimulation (HFS). In conjunction with altered STIM1 splicing in human Alzheimer disease, our findings highlight STIM1 splicing as an important regulator of neuronal calcium homeostasis and of synaptic plasticity.

Keywords: CICR; ICRAC; Orai; SOCE; endocytosis; localization; presynaptic ER; short-term enhancement; vesicles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Membrane / metabolism
  • Endoplasmic Reticulum / metabolism
  • Exons / genetics
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Neurons / metabolism
  • ORAI1 Protein / metabolism
  • Phenotype
  • Presynaptic Terminals / metabolism
  • Protein Domains
  • Protein Isoforms / chemistry
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA Splicing / genetics
  • Signal Transduction
  • Stromal Interaction Molecule 1 / chemistry
  • Stromal Interaction Molecule 1 / genetics
  • Stromal Interaction Molecule 1 / metabolism*
  • Synapses / metabolism*

Substances

  • ORAI1 Protein
  • Protein Isoforms
  • Stromal Interaction Molecule 1