Netrin-G2 dysfunction causes a Rett-like phenotype with areflexia

Hum Mutat. 2020 Feb;41(2):476-486. doi: 10.1002/humu.23945. Epub 2019 Nov 15.

Abstract

We describe the underlying genetic cause of a novel Rett-like phenotype accompanied by areflexia in three methyl-CpG-binding protein 2-negative individuals from two unrelated families. Discovery analysis was performed using whole-exome sequencing followed by Sanger sequencing for validation and segregation. Functional studies using short-hairpin RNA for targeted gene knockdown were implemented by the transfection of mouse cultured primary hippocampal neurons and in vivo by in utero electroporation. All patients shared a common homozygous frameshift mutation (chr9:135073515, c.376dupT, p.(Ser126PhefsTer241)) in netrin-G2 (NTNG2, NM_032536.3) with predicted nonsense-mediated decay. The mutation fully segregated with the disease in both families. The knockdown of either NTNG2 or the related netrin-G family member NTNG1 resulted in severe neurodevelopmental defects of neuronal morphology and migration. While NTNG1 has previously been linked to a Rett syndrome (RTT)-like phenotype, this is the first description of a RTT-like phenotype caused by NTNG2 mutation. Netrin-G proteins have been shown to be required for proper axonal guidance during early brain development and involved in N-methyl- d-aspartate-mediated synaptic transmission. Our results demonstrating that knockdown of murine NTNG2 causes severe impairments of neuronal morphology and cortical migration are consistent with those of RTT animal models and the shared neurodevelopmental phenotypes between the individuals described here and typical RTT patients.

Keywords: NTNG2; RTT-like; Rett; areflexia; developmental delay; netrin-G.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Charcot-Marie-Tooth Disease / diagnosis*
  • Charcot-Marie-Tooth Disease / genetics*
  • Child
  • Child, Preschool
  • Consanguinity
  • Disease Models, Animal
  • Exome Sequencing
  • Facies
  • Female
  • GPI-Linked Proteins / genetics*
  • Genetic Association Studies* / methods
  • Genetic Predisposition to Disease*
  • Humans
  • Male
  • Mice
  • Netrins / genetics*
  • Neurons / metabolism
  • Phenotype
  • Rett Syndrome / diagnosis*
  • Rett Syndrome / genetics*
  • Sequence Analysis, DNA

Substances

  • GPI-Linked Proteins
  • NTNG1 protein, human
  • NTNG2 protein, human
  • Netrins