De novo pathogenic variants in neuronal differentiation factor 2 (NEUROD2) cause a form of early infantile epileptic encephalopathy

J Med Genet. 2019 Feb;56(2):113-122. doi: 10.1136/jmedgenet-2018-105322. Epub 2018 Oct 15.

Abstract

Background: Early infantile epileptic encephalopathies are severe disorders consisting of early-onset refractory seizures accompanied often by significant developmental delay. The increasing availability of next-generation sequencing has facilitated the recognition of single gene mutations as an underlying aetiology of some forms of early infantile epileptic encephalopathies.

Objectives: This study was designed to identify candidate genes as a potential cause of early infantile epileptic encephalopathy, and then to provide genetic and functional evidence supporting patient variants as causative.

Methods: We used whole exome sequencing to identify candidate genes. To model the disease and assess the functional effects of patient variants on candidate protein function, we used in vivo CRISPR/Cas9-mediated genome editing and protein overexpression in frog tadpoles.

Results: We identified novel de novo variants in neuronal differentiation factor 2 (NEUROD2) in two unrelated children with early infantile epileptic encephalopathy. Depleting neurod2 with CRISPR/Cas9-mediated genome editing induced spontaneous seizures in tadpoles, mimicking the patients' condition. Overexpression of wild-type NEUROD2 induced ectopic neurons in tadpoles; however, patient variants were markedly less effective, suggesting that both variants are dysfunctional and likely pathogenic.

Conclusion: This study provides clinical and functional support for NEUROD2 variants as a cause of early infantile epileptic encephalopathy, the first evidence of human disease caused by NEUROD2 variants.

Keywords: epilepsy and seizures; epileptic encephalopathy; neurod2; neuronal differentiation factor; xenopus.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • CRISPR-Cas Systems
  • Child, Preschool
  • Exome Sequencing
  • Female
  • Gene Expression
  • Gene Knockdown Techniques
  • Humans
  • Larva / genetics
  • Magnetic Resonance Imaging
  • Male
  • Mutation, Missense
  • Neuropeptides / genetics*
  • Spasms, Infantile / diagnostic imaging
  • Spasms, Infantile / etiology
  • Spasms, Infantile / genetics*
  • Xenopus laevis / embryology
  • Xenopus laevis / genetics

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • NEUROD2 protein, human
  • Neuropeptides

Supplementary concepts

  • Infantile Epileptic-Dyskinetic Encephalopathy