Integrity and regeneration of mechanotransduction machinery regulate aminoglycoside entry and sensory cell death

PLoS One. 2013;8(1):e54794. doi: 10.1371/journal.pone.0054794. Epub 2013 Jan 24.

Abstract

Sound perception requires functional hair cell mechanotransduction (MET) machinery, including the MET channels and tip-link proteins. Prior work showed that uptake of ototoxic aminoglycosides (AG) into hair cells requires functional MET channels. In this study, we examined whether tip-link proteins, including Cadherin 23 (Cdh23), regulate AG entry into hair cells. Using time-lapse microscopy on cochlear explants, we found rapid uptake of gentamicin-conjugated Texas Red (GTTR) into hair cells from three-day-old Cdh23(+/+) and Cdh23(v2J/+) mice, but failed to detect GTTR uptake in Cdh23(v2J/v2J) hair cells. Pre-treatment of wildtype cochleae with the calcium chelator 1,2-bis(o-aminophenoxy) ethane-N,N,N',N'-tetraacetic acid (BAPTA) to disrupt tip-links also effectively reduced GTTR uptake into hair cells. Both Cdh23(v2J/v2J) and BAPTA-treated hair cells were protected from degeneration caused by gentamicin. Six hours after BAPTA treatment, GTTR uptake remained reduced in comparison to controls; by 24 hours, drug uptake was comparable between untreated and BAPTA-treated hair cells, which again became susceptible to cell death induced by gentamicin. Together, these results provide genetic and pharmacologic evidence that tip-links are required for AG uptake and toxicity in hair cells. Because tip-links can spontaneously regenerate, their temporary breakage offers a limited time window when hair cells are protected from AG toxicity.

Publication types

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

MeSH terms

  • Aminoglycosides / metabolism*
  • Animals
  • Cadherins / genetics
  • Cadherins / physiology
  • Calcium / metabolism
  • Cell Death
  • Chelating Agents / metabolism
  • Egtazic Acid / analogs & derivatives
  • Hair Cells, Auditory / metabolism
  • Mechanotransduction, Cellular*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutation

Substances

  • Aminoglycosides
  • Cadherins
  • Cdh23 protein, mouse
  • Chelating Agents
  • Egtazic Acid
  • 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid
  • Calcium