The novel mouse mutation Oblivion inactivates the PMCA2 pump and causes progressive hearing loss

PLoS Genet. 2008 Oct;4(10):e1000238. doi: 10.1371/journal.pgen.1000238. Epub 2008 Oct 31.

Abstract

Progressive hearing loss is common in the human population, but we have few clues to the molecular basis. Mouse mutants with progressive hearing loss offer valuable insights, and ENU (N-ethyl-N-nitrosourea) mutagenesis is a useful way of generating models. We have characterised a new ENU-induced mouse mutant, Oblivion (allele symbol Obl), showing semi-dominant inheritance of hearing impairment. Obl/+ mutants showed increasing hearing impairment from post-natal day (P)20 to P90, and loss of auditory function was followed by a corresponding base to apex progression of hair cell degeneration. Obl/Obl mutants were small, showed severe vestibular dysfunction by 2 weeks of age, and were completely deaf from birth; sensory hair cells were completely degenerate in the basal turn of the cochlea, although hair cells appeared normal in the apex. We mapped the mutation to Chromosome 6. Mutation analysis of Atp2b2 showed a missense mutation (2630C-->T) in exon 15, causing a serine to phenylalanine substitution (S877F) in transmembrane domain 6 of the PMCA2 pump, the resident Ca(2+) pump of hair cell stereocilia. Transmembrane domain mutations in these pumps generally are believed to be incompatible with normal targeting of the protein to the plasma membrane. However, analyses of hair cells in cultured utricular maculae of Obl/Obl mice and of the mutant Obl pump in model cells showed that the protein was correctly targeted to the plasma membrane. Biochemical and biophysical characterisation showed that the pump had lost a significant portion of its non-stimulated Ca(2+) exporting ability. These findings can explain the progressive loss of auditory function, and indicate the limits in our ability to predict mechanism from sequence alone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aequorin / metabolism
  • Amino Acid Substitution
  • Animals
  • Calcium / metabolism*
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Chromosome Mapping
  • DNA Mutational Analysis
  • Deafness / genetics*
  • Deafness / pathology
  • Deafness / physiopathology
  • Ear, Inner / pathology
  • Ear, Inner / ultrastructure
  • Evoked Potentials, Auditory, Brain Stem
  • Hair Cells, Auditory / metabolism*
  • Hair Cells, Auditory / pathology
  • Mice
  • Microscopy, Electron, Scanning
  • Mutagenesis
  • Mutation, Missense*
  • Plasma Membrane Calcium-Transporting ATPases / genetics*
  • Plasma Membrane Calcium-Transporting ATPases / metabolism*
  • Saccule and Utricle / metabolism

Substances

  • Aequorin
  • Plasma Membrane Calcium-Transporting ATPases
  • Atp2b2 protein, mouse
  • Calcium