Cingulin regulates hair cell cuticular plate morphology and is required for hearing in human and mouse

EMBO Mol Med. 2023 Nov 8;15(11):e17611. doi: 10.15252/emmm.202317611. Epub 2023 Sep 11.

Abstract

Cingulin (CGN) is a cytoskeleton-associated protein localized at the apical junctions of epithelial cells. CGN interacts with major cytoskeletal filaments and regulates RhoA activity. However, physiological roles of CGN in development and human diseases are currently unknown. Here, we report a multi-generation family presenting with autosomal dominant non-syndromic hearing loss (ADNSHL) that co-segregates with a CGN heterozygous truncating variant, c.3330delG (p.Leu1110Leufs*17). CGN is normally expressed at the apical cell junctions of the organ of Corti, with enriched localization at hair cell cuticular plates and circumferential belts. In mice, the putative disease-causing mutation results in reduced expression and abnormal subcellular localization of the CGN protein, abolishes its actin polymerization activity, and impairs the normal morphology of hair cell cuticular plates and hair bundles. Hair cell-specific Cgn knockout leads to high-frequency hearing loss. Importantly, Cgn mutation knockin mice display noise-sensitive, progressive hearing loss and outer hair cell degeneration. In summary, we identify CGN c.3330delG as a pathogenic variant for ADNSHL and reveal essential roles of CGN in the maintenance of cochlear hair cell structures and auditory function.

Keywords: ADNSHL; cingulin; cuticular plate; hair cells; hearing loss.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cytoskeletal Proteins
  • Deafness* / genetics
  • Hair Cells, Auditory / metabolism
  • Hearing / physiology
  • Hearing Loss* / genetics
  • Hearing Loss* / metabolism
  • Humans
  • Mice

Substances

  • Cytoskeletal Proteins
  • Cgn protein, mouse
  • CGN protein, human

Supplementary concepts

  • Nonsyndromic Deafness

Associated data

  • SRA/SRP449242