A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins

Neuron. 2005 Oct 20;48(2):229-36. doi: 10.1016/j.neuron.2005.08.026.

Abstract

Previous studies suggested that postsynaptic neuroligins form a trans-synaptic complex with presynaptic beta-neurexins, but not with presynaptic alpha-neurexins. Unexpectedly, we now find that neuroligins also bind alpha-neurexins and that alpha- and beta-neurexin binding by neuroligin 1 is regulated by alternative splicing of neuroligin 1 (at splice site B) and of neurexins (at splice site 4). In neuroligin 1, splice site B is a master switch that determines alpha-neurexin binding but leaves beta-neurexin binding largely unaffected, whereas alternative splicing of neurexins modulates neuroligin binding. Moreover, neuroligin 1 splice variants with distinct neurexin binding properties differentially regulate synaptogenesis: neuroligin 1 that binds only beta-neurexins potently stimulates synapse formation, whereas neuroligin 1 that binds to both alpha- and beta-neurexins more effectively promotes synapse expansion. These findings suggest that neuroligin binding to alpha- and beta-neurexins mediates trans-synaptic cell adhesion but has distinct effects on synapse formation, indicating that expression of different neuroligin and neurexin isoforms specifies a trans-synaptic signaling code.

Publication types

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

MeSH terms

  • Alternative Splicing*
  • Animals
  • Animals, Newborn
  • Blotting, Western / methods
  • Cell Adhesion / physiology
  • Cell Adhesion Molecules, Neuronal
  • Cells, Cultured
  • Chromatography, Affinity / methods
  • Electrophoretic Mobility Shift Assay / methods
  • Glycoproteins / classification
  • Glycoproteins / metabolism*
  • Green Fluorescent Proteins / metabolism
  • Hippocampus / cytology*
  • Humans
  • Immunohistochemistry / methods
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Microtubule-Associated Proteins / metabolism
  • Mutagenesis / physiology
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / metabolism*
  • Neuropeptides / classification
  • Neuropeptides / metabolism*
  • Protein Binding / physiology
  • Rats
  • Recombinant Proteins / biosynthesis
  • Synapses / metabolism*
  • Synapsins / metabolism
  • Transfection / methods

Substances

  • Cell Adhesion Molecules, Neuronal
  • Glycoproteins
  • MAP2 protein, rat
  • Membrane Proteins
  • Microtubule-Associated Proteins
  • Nerve Tissue Proteins
  • Neuropeptides
  • Recombinant Proteins
  • Synapsins
  • enhanced green fluorescent protein
  • neurexophilin
  • neuroligin 1
  • Green Fluorescent Proteins