Loss-of-function variants in the KCNQ5 gene are implicated in genetic generalized epilepsies

EBioMedicine. 2022 Oct:84:104244. doi: 10.1016/j.ebiom.2022.104244. Epub 2022 Sep 9.

Abstract

Background: De novo missense variants in KCNQ5, encoding the voltage-gated K+ channel KV7.5, have been described to cause developmental and epileptic encephalopathy (DEE) or intellectual disability (ID). We set out to identify disease-related KCNQ5 variants in genetic generalized epilepsy (GGE) and their underlying mechanisms.

Methods: 1292 families with GGE were studied by next-generation sequencing. Whole-cell patch-clamp recordings, biotinylation and phospholipid overlay assays were performed in mammalian cells combined with homology modelling.

Findings: We identified three deleterious heterozygous missense variants, one truncation and one splice site alteration in five independent families with GGE with predominant absence seizures; two variants were also associated with mild to moderate ID. All missense variants displayed a strongly decreased current density indicating a loss-of-function (LOF). When mutant channels were co-expressed with wild-type (WT) KV7.5 or KV7.5 and KV7.3 channels, three variants also revealed a significant dominant-negative effect on WT channels. Other gating parameters were unchanged. Biotinylation assays indicated a normal surface expression of the variants. The R359C variant altered PI(4,5)P2-interaction.

Interpretation: Our study identified deleterious KCNQ5 variants in GGE, partially combined with mild to moderate ID. The disease mechanism is a LOF partially with dominant-negative effects through functional deficits. LOF of KV7.5 channels will reduce the M-current, likely resulting in increased excitability of KV7.5-expressing neurons. Further studies on network level are necessary to understand which circuits are affected and how this induces generalized seizures.

Funding: DFG/FNR Research Unit FOR-2715 (Germany/Luxemburg), BMBF rare disease network Treat-ION (Germany), foundation 'no epilep' (Germany).

Keywords: Exome sequencing; Genetic generalized epilepsy; KCNQ5; Loss-of-function; Patch-clamp.

MeSH terms

  • Animals
  • Epilepsy* / genetics
  • Epilepsy, Generalized* / diagnosis
  • Epilepsy, Generalized* / genetics
  • Humans
  • Intellectual Disability* / genetics
  • Mammals
  • Mutation
  • Phospholipids

Substances

  • Phospholipids