CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses

Nat Neurosci. 2014 Jan;17(1):56-64. doi: 10.1038/nn.3601. Epub 2013 Dec 15.

Abstract

Neuroligins are postsynaptic cell adhesion molecules that are important for synaptic function through their trans-synaptic interaction with neurexins (NRXNs). The localization and synaptic effects of neuroligin-1 (NL-1, also called NLGN1) are specific to excitatory synapses with the capacity to enhance excitatory synapses dependent on synaptic activity or Ca(2+)/calmodulin kinase II (CaMKII). Here we report that CaMKII robustly phosphorylates the intracellular domain of NL-1. We show that T739 is the dominant CaMKII site on NL-1 and is phosphorylated in response to synaptic activity in cultured rodent neurons and sensory experience in vivo. Furthermore, a phosphodeficient mutant (NL-1 T739A) reduces the basal and activity-driven surface expression of NL-1, leading to a reduction in neuroligin-mediated excitatory synaptic potentiation. To the best of our knowledge, our results are the first to demonstrate a direct functional interaction between CaMKII and NL-1, two primary components of excitatory synapses.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Animals, Newborn
  • Benzylamines / pharmacology
  • Bicuculline / pharmacology
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cell Adhesion Molecules, Neuronal / genetics
  • Cell Adhesion Molecules, Neuronal / metabolism*
  • Cells, Cultured
  • Disks Large Homolog 4 Protein
  • Dose-Response Relationship, Drug
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / genetics
  • Excitatory Postsynaptic Potentials / physiology*
  • Female
  • GABA Antagonists / pharmacology
  • Gene Expression Regulation / genetics
  • Guanylate Kinases / metabolism
  • Hippocampus / cytology
  • Humans
  • Immunoprecipitation
  • In Vitro Techniques
  • Luminescent Proteins / genetics
  • Male
  • Mass Spectrometry
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / pharmacology
  • Mutation / genetics
  • Neurons / drug effects
  • Neurons / physiology*
  • Patch-Clamp Techniques
  • Phosphorylation / genetics
  • Protein Kinase Inhibitors / pharmacology
  • Receptors, AMPA / genetics
  • Sensory Deprivation / physiology
  • Sequence Analysis, Protein
  • Statistics, Nonparametric
  • Sulfonamides / pharmacology
  • Synapses / physiology*
  • Transfection
  • Vesicular Glutamate Transport Protein 1 / metabolism
  • Visual Cortex / metabolism

Substances

  • Benzylamines
  • Cell Adhesion Molecules, Neuronal
  • Disks Large Homolog 4 Protein
  • Dlg4 protein, mouse
  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • KN 92
  • Luminescent Proteins
  • Membrane Proteins
  • MicroRNAs
  • Protein Kinase Inhibitors
  • Receptors, AMPA
  • Sulfonamides
  • Vesicular Glutamate Transport Protein 1
  • neuroligin 1
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Guanylate Kinases
  • glutamate receptor ionotropic, AMPA 1
  • Bicuculline