STON2 variations are involved in synaptic dysfunction and schizophrenia-like behaviors by regulating Syt1 trafficking

Sci Bull (Beijing). 2024 May 30;69(10):1458-1471. doi: 10.1016/j.scib.2024.02.013. Epub 2024 Feb 13.

Abstract

Synaptic dysfunction is a core component of the pathophysiology of schizophrenia. However, the genetic risk factors and molecular mechanisms related to synaptic dysfunction are still not fully understood. The Stonin 2 (STON2) gene encodes a major adaptor for clathrin-mediated endocytosis (CME) of synaptic vesicles. In this study, we showed that the C-C (307Pro-851Ala) haplotype of STON2 increases the susceptibility to schizophrenia and examined whether STON2 variations cause schizophrenia-like behaviors through the regulation of CME. We found that schizophrenia-related STON2 variations led to protein dephosphorylation, which affected its interaction with synaptotagmin 1 (Syt1), a calcium sensor protein located in the presynaptic membrane that is critical for CME. STON2307Pro851Ala knockin mice exhibited deficits in synaptic transmission, short-term plasticity, and schizophrenia-like behaviors. Moreover, among seven antipsychotic drugs, patients with the C-C (307Pro-851Ala) haplotype responded better to haloperidol than did the T-A (307Ser-851Ser) carriers. The recovery of deficits in Syt1 sorting and synaptic transmission by acute administration of haloperidol effectively improved schizophrenia-like behaviors in STON2307Pro851Ala knockin mice. Our findings demonstrated the effect of schizophrenia-related STON2 variations on synaptic dysfunction through the regulation of CME, which might be attractive therapeutic targets for treating schizophrenia-like phenotypes.

Keywords: Haloperidol; STON2 variations; Schizophrenia; Synaptic dysfunction; Syt1.

MeSH terms

  • Animals
  • Antipsychotic Agents / pharmacology
  • Antipsychotic Agents / therapeutic use
  • Endocytosis / drug effects
  • Female
  • Gene Knock-In Techniques
  • Genetic Predisposition to Disease
  • Haloperidol / pharmacology
  • Haplotypes
  • Humans
  • Male
  • Mice
  • Phosphorylation
  • Protein Transport
  • Schizophrenia* / genetics
  • Schizophrenia* / metabolism
  • Synapses / drug effects
  • Synapses / metabolism
  • Synaptic Transmission* / drug effects
  • Synaptic Vesicles / metabolism
  • Synaptotagmin I* / genetics
  • Synaptotagmin I* / metabolism

Substances

  • Antipsychotic Agents
  • Haloperidol
  • Synaptotagmin I
  • SYT1 protein, human
  • Syt1 protein, mouse
  • stonin 2 protein, mouse