De novo variants in SP9 cause a novel form of interneuronopathy characterized by intellectual disability, autism spectrum disorder, and epilepsy with variable expressivity

Genet Med. 2024 May;26(5):101087. doi: 10.1016/j.gim.2024.101087. Epub 2024 Jan 27.

Abstract

Purpose: Interneuronopathies are a group of neurodevelopmental disorders characterized by deficient migration and differentiation of gamma-aminobutyric acidergic interneurons resulting in a broad clinical spectrum, including autism spectrum disorders, early-onset epileptic encephalopathy, intellectual disability, and schizophrenic disorders. SP9 is a transcription factor belonging to the Krüppel-like factor and specificity protein family, the members of which harbor highly conserved DNA-binding domains. SP9 plays a central role in interneuron development and tangential migration, but it has not yet been implicated in a human neurodevelopmental disorder.

Methods: Cases with SP9 variants were collected through international data-sharing networks. To address the specific impact of SP9 variants, in silico and in vitro assays were carried out.

Results: De novo heterozygous variants in SP9 cause a novel form of interneuronopathy. SP9 missense variants affecting the glutamate 378 amino acid result in severe epileptic encephalopathy because of hypomorphic and neomorphic DNA-binding effects, whereas SP9 loss-of-function variants result in a milder phenotype with epilepsy, developmental delay, and autism spectrum disorder.

Conclusion: De novo heterozygous SP9 variants are responsible for a neurodevelopmental disease. Interestingly, variants located in conserved DNA-binding domains of KLF/SP family transcription factors may lead to neomorphic DNA-binding functions resulting in a combination of loss- and gain-of-function effects.

Keywords: Interneuronopathy; KLF/SP transcription factor; Neomorphic DNA-binding functions; Neurodevelopmental disorders; SP9.

Publication types

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

MeSH terms

  • Adolescent
  • Autism Spectrum Disorder* / genetics
  • Autism Spectrum Disorder* / pathology
  • Child
  • Child, Preschool
  • Epilepsy* / genetics
  • Epilepsy* / pathology
  • Female
  • Heterozygote
  • Humans
  • Intellectual Disability* / genetics
  • Intellectual Disability* / pathology
  • Interneurons* / metabolism
  • Interneurons* / pathology
  • Male
  • Mutation, Missense / genetics
  • Neurodevelopmental Disorders / genetics
  • Neurodevelopmental Disorders / pathology
  • Phenotype
  • Sp Transcription Factors* / genetics
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • Sp Transcription Factors