A nonsense TMEM43 variant leads to disruption of connexin-linked function and autosomal dominant auditory neuropathy spectrum disorder

Proc Natl Acad Sci U S A. 2021 Jun 1;118(22):e2019681118. doi: 10.1073/pnas.2019681118.

Abstract

Genes that are primarily expressed in cochlear glia-like supporting cells (GLSs) have not been clearly associated with progressive deafness. Herein, we present a deafness locus mapped to chromosome 3p25.1 and an auditory neuropathy spectrum disorder (ANSD) gene, TMEM43, mainly expressed in GLSs. We identify p.(Arg372Ter) of TMEM43 by linkage analysis and exome sequencing in two large Asian families segregating ANSD, which is characterized by inability to discriminate speech despite preserved sensitivity to sound. The knock-in mouse with the p.(Arg372Ter) variant recapitulates a progressive hearing loss with histological abnormalities in GLSs. Mechanistically, TMEM43 interacts with the Connexin26 and Connexin30 gap junction channels, disrupting the passive conductance current in GLSs in a dominant-negative fashion when the p.(Arg372Ter) variant is introduced. Based on these mechanistic insights, cochlear implant was performed on three subjects, and speech discrimination was successfully restored. Our study highlights a pathological role of cochlear GLSs by identifying a deafness gene and its causal relationship with ANSD.

Keywords: auditory neuropathy spectrum disorder; cochlea; connexins; glia-like supporting cells.

Publication types

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

MeSH terms

  • Animals
  • Cochlear Implantation
  • Codon, Nonsense*
  • Connexins / metabolism*
  • Female
  • Genes, Dominant*
  • Hearing Loss, Central / genetics*
  • Hearing Loss, Central / metabolism
  • Hearing Loss, Central / physiopathology
  • Hearing Loss, Central / surgery
  • Humans
  • Male
  • Membrane Proteins / genetics*
  • Mice
  • Mice, Inbred C57BL
  • Pedigree
  • Speech Perception

Substances

  • Codon, Nonsense
  • Connexins
  • Membrane Proteins
  • TMEM43 protein, human

Supplementary concepts

  • Auditory neuropathy