SALM1 controls synapse development by promoting F-actin/PIP2-dependent Neurexin clustering

EMBO J. 2019 Sep 2;38(17):e101289. doi: 10.15252/embj.2018101289. Epub 2019 Aug 1.

Abstract

Synapse development requires spatiotemporally regulated recruitment of synaptic proteins. In this study, we describe a novel presynaptic mechanism of cis-regulated oligomerization of adhesion molecules that controls synaptogenesis. We identified synaptic adhesion-like molecule 1 (SALM1) as a constituent of the proposed presynaptic Munc18/CASK/Mint1/Lin7b organizer complex. SALM1 preferentially localized to presynaptic compartments of excitatory hippocampal neurons. SALM1 depletion in excitatory hippocampal primary neurons impaired Neurexin1β- and Neuroligin1-mediated excitatory synaptogenesis and reduced synaptic vesicle clustering, synaptic transmission, and synaptic vesicle release. SALM1 promoted Neurexin1β clustering in an F-actin- and PIP2-dependent manner. Two basic residues in SALM1's juxtamembrane polybasic domain are essential for this clustering. Together, these data show that SALM1 is a presynaptic organizer of synapse development by promoting F-actin/PIP2-dependent clustering of Neurexin.

Keywords: PIP2; SALM1; neurexin; synapse organization; synaptogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Animals
  • Calcium-Binding Proteins / metabolism*
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Cells, Cultured
  • HEK293 Cells
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Humans
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neural Cell Adhesion Molecules / metabolism*
  • Neurogenesis
  • Phosphatidylinositol 4,5-Diphosphate / metabolism*
  • Synapses / metabolism*

Substances

  • Actins
  • Calcium-Binding Proteins
  • Cell Adhesion Molecules, Neuronal
  • Lrfn2 protein, mouse
  • Membrane Glycoproteins
  • Nerve Tissue Proteins
  • Neural Cell Adhesion Molecules
  • Nrxn1 protein, mouse
  • Phosphatidylinositol 4,5-Diphosphate
  • neuroligin 1