Endothelium-Derived Semaphorin 3G Regulates Hippocampal Synaptic Structure and Plasticity via Neuropilin-2/PlexinA4

Neuron. 2019 Mar 6;101(5):920-937.e13. doi: 10.1016/j.neuron.2018.12.036. Epub 2019 Jan 23.

Abstract

The proper interactions between blood vessels and neurons are critical for maintaining the strength of neural circuits and cognitive function. However, the precise molecular events underlying these interactions remain largely unknown. Here, we report that the selective knockout of semaphorin 3G (Sema3G) in endothelial cells impaired hippocampal-dependent memory and reduced dendritic spine density in CA1 neurons in mice; these effects were reversed after restoration of Sema3G levels in the hippocampus by AAV transfection. We further show that Sema3G increased excitatory synapse density via neuropilin-2/PlexinA4 signaling and through activation of Rac1. These results provide the first evidence that, in the central nervous system, endothelial Sema3G serves as a vascular-derived synaptic organizer that regulates synaptic plasticity and hippocampal-dependent memory. Our findings highlight the role of vascular endothelial cells in regulating cognitive function through intercellular communication with neurons in the hippocampus.

Keywords: Nrp2; PlexinA4; Semaphorin 3G; endothelial cell; hippocampus; neurovascular interaction; synaptic plasticity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Endothelium, Vascular / metabolism*
  • Female
  • HEK293 Cells
  • Hippocampus / metabolism*
  • Hippocampus / physiology
  • Humans
  • Male
  • Memory Disorders / genetics
  • Memory Disorders / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neuronal Plasticity*
  • Neuropilin-2 / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism
  • Semaphorins / genetics
  • Semaphorins / metabolism*
  • Synapses / metabolism
  • Synapses / physiology

Substances

  • Nerve Tissue Proteins
  • Neuropilin-2
  • Plxna4 protein, mouse
  • Receptors, Cell Surface
  • Semaphorins
  • semaphorin 3G, mouse