Human Neuropsychiatric Disease Modeling using Conditional Deletion Reveals Synaptic Transmission Defects Caused by Heterozygous Mutations in NRXN1

Cell Stem Cell. 2015 Sep 3;17(3):316-28. doi: 10.1016/j.stem.2015.07.017. Epub 2015 Aug 13.

Abstract

Heterozygous mutations of the NRXN1 gene, which encodes the presynaptic cell-adhesion molecule neurexin-1, were repeatedly associated with autism and schizophrenia. However, diverse clinical presentations of NRXN1 mutations in patients raise the question of whether heterozygous NRXN1 mutations alone directly impair synaptic function. To address this question under conditions that precisely control for genetic background, we generated human ESCs with different heterozygous conditional NRXN1 mutations and analyzed two different types of isogenic control and NRXN1 mutant neurons derived from these ESCs. Both heterozygous NRXN1 mutations selectively impaired neurotransmitter release in human neurons without changing neuronal differentiation or synapse formation. Moreover, both NRXN1 mutations increased the levels of CASK, a critical synaptic scaffolding protein that binds to neurexin-1. Our results show that, unexpectedly, heterozygous inactivation of NRXN1 directly impairs synaptic function in human neurons, and they illustrate the value of this conditional deletion approach for studying the functional effects of disease-associated mutations.

Keywords: autism; human neurons; iN cells; neurexin; schizophrenia; synapse; synaptic cell adhesion.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Calcium-Binding Proteins
  • Cell Adhesion Molecules, Neuronal / chemistry
  • Cell Adhesion Molecules, Neuronal / genetics*
  • Cell Differentiation
  • Cell Membrane / metabolism
  • Enzyme Stability
  • Gene Knockout Techniques
  • Gene Targeting
  • Guanylate Kinases / metabolism
  • Heterozygote
  • Human Embryonic Stem Cells / cytology
  • Human Embryonic Stem Cells / metabolism
  • Humans
  • Mental Disorders / genetics*
  • Miniature Postsynaptic Potentials
  • Models, Biological*
  • Molecular Sequence Data
  • Mutation / genetics*
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / genetics*
  • Neural Cell Adhesion Molecules
  • Neurons / cytology
  • Neurotransmitter Agents / metabolism
  • Phenotype
  • Synapses / metabolism
  • Synaptic Transmission*
  • Synaptic Vesicles / metabolism

Substances

  • Calcium-Binding Proteins
  • Cell Adhesion Molecules, Neuronal
  • NRXN1 protein, human
  • Nerve Tissue Proteins
  • Neural Cell Adhesion Molecules
  • Neurotransmitter Agents
  • CASK kinases
  • Guanylate Kinases