Functional analysis of rare variants found in schizophrenia implicates a critical role for GIT1-PAK3 signaling in neuroplasticity

Mol Psychiatry. 2017 Mar;22(3):417-429. doi: 10.1038/mp.2016.98. Epub 2016 Jul 26.

Abstract

Although the pathogenesis of schizophrenia (SCZ) is proposed to involve alterations of neural circuits via synaptic dysfunction, the underlying molecular mechanisms remain poorly understood. Recent exome sequencing studies of SCZ have uncovered numerous single-nucleotide variants (SNVs); however, the majority of these SNVs have unknown functional consequences, leaving their disease relevance uncertain. Filling this knowledge gap requires systematic application of quantitative and scalable assays to assess known and novel biological functions of genes. Here we demonstrate loss-of-function effects of multiple rare coding SNVs found in SCZ subjects in the GIT1 (G protein-coupled receptor kinase interacting ArfGAP 1) gene using functional cell-based assays involving coexpression of GIT1 and PAK3 (p21 protein (Cdc42/Rac)-activated kinase 3). Most notably, a GIT1-R283W variant reported in four independent SCZ cases was defective in activating PAK3 as well as MAPK (mitogen-activated protein kinase). Similar functional deficits were found for a de novo SCZ variant GIT1-S601N. Additional assays revealed deficits in the capacity of GIT1-R283W to stimulate PAK phosphorylation in cultured hippocampal neurons. In addition, GIT1-R283W showed deficits in the induction of GAD1 (glutamate decarboxylase 1) protein expression. Extending these functional assays to 10 additional rare GIT1 variants revealed the existence of an allelic series with the majority of the SCZ case variants exhibiting loss of function toward MAPK activation in a manner correlated with loss of PAK3 activation. Taken together, we propose that rare variants in GIT1, along with other genetic and environmental factors, cause dysregulation of PAK3 leading to synaptic deficits in SCZ.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Cell Culture Techniques / methods
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • GTPase-Activating Proteins / genetics
  • Genetic Variation / genetics
  • Guanine Nucleotide Exchange Factors / metabolism
  • HEK293 Cells / metabolism
  • Hippocampus / metabolism
  • Humans
  • Mitogen-Activated Protein Kinases / metabolism
  • Neuronal Plasticity / genetics
  • Neuronal Plasticity / physiology
  • Neurons / metabolism
  • Phosphoproteins
  • Phosphorylation
  • Polymorphism, Single Nucleotide / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Schizophrenia / genetics
  • Signal Transduction / genetics
  • p21-Activated Kinases / genetics
  • p21-Activated Kinases / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Cell Cycle Proteins
  • GIT1 protein, human
  • GTPase-Activating Proteins
  • Guanine Nucleotide Exchange Factors
  • Phosphoproteins
  • Protein Serine-Threonine Kinases
  • p21-Activated Kinases
  • Mitogen-Activated Protein Kinases