Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses

Nat Neurosci. 2009 Apr;12(4):428-37. doi: 10.1038/nn.2279. Epub 2009 Mar 1.

Abstract

Synaptic adhesion molecules regulate multiple steps of synapse formation and maturation. The great diversity of neuronal synapses predicts the presence of a large number of adhesion molecules that control synapse formation through trans-synaptic and heterophilic adhesion. We identified a previously unknown trans-synaptic interaction between netrin-G ligand-3 (NGL-3), a postsynaptic density (PSD) 95-interacting postsynaptic adhesion molecule, and leukocyte common antigen-related (LAR), a receptor protein tyrosine phosphatase. NGL-3 and LAR expressed in heterologous cells induced pre- and postsynaptic differentiation in contacting axons and dendrites of cocultured rat hippocampal neurons, respectively. Neuronal overexpression of NGL-3 increased presynaptic contacts on dendrites of transfected neurons. Direct aggregation of NGL-3 on dendrites induced coclustering of excitatory postsynaptic proteins. Knockdown of NGL-3 reduced the number and function of excitatory synapses. Competitive inhibition by soluble LAR reduced NGL-3-induced presynaptic differentiation. These results suggest that the trans-synaptic adhesion between NGL-3 and LAR regulates excitatory synapse formation in a bidirectional manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / physiology*
  • Cell Differentiation / physiology
  • Cells, Cultured
  • Coculture Techniques / methods
  • Embryo, Mammalian
  • Gene Expression Regulation, Developmental / physiology
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology
  • Humans
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons / cytology*
  • Presynaptic Terminals / metabolism
  • Rats
  • Receptor-Like Protein Tyrosine Phosphatases, Class 2 / genetics
  • Receptor-Like Protein Tyrosine Phosphatases, Class 2 / physiology*
  • Receptors, Cell Surface / genetics
  • Synapses / classification
  • Synapses / physiology*
  • Synaptic Transmission / genetics
  • Synaptic Transmission / physiology*
  • Transfection / methods
  • Vesicular Inhibitory Amino Acid Transport Proteins / metabolism

Substances

  • Cell Adhesion Molecules
  • LRRC4C protein, human
  • Nerve Tissue Proteins
  • Receptors, Cell Surface
  • Slc32a1 protein, rat
  • Vesicular Inhibitory Amino Acid Transport Proteins
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Receptor-Like Protein Tyrosine Phosphatases, Class 2