A novel role of cytosolic protein synthesis inhibition in aminoglycoside ototoxicity

J Neurosci. 2013 Feb 13;33(7):3079-93. doi: 10.1523/JNEUROSCI.3430-12.2013.

Abstract

Ototoxicity is a main dose-limiting factor in the clinical application of aminoglycoside antibiotics. Despite longstanding research efforts, our understanding of the mechanisms underlying aminoglycoside ototoxicity remains limited. Here we report the discovery of a novel stress pathway that contributes to aminoglycoside-induced hair cell degeneration. Modifying the previously developed bioorthogonal noncanonical amino acid tagging method, we used click chemistry to study the role of protein synthesis activity in aminoglycoside-induced hair cell stress. We demonstrate that aminoglycosides inhibit protein synthesis in hair cells and activate a signaling pathway similar to ribotoxic stress response, contributing to hair cell degeneration. The ability of a particular aminoglycoside to inhibit protein synthesis and to activate the c-Jun N-terminal kinase (JNK) pathway correlated well with its ototoxic potential. Finally, we report that a Food and Drug Administration-approved drug known to inhibit ribotoxic stress response also prevents JNK activation and improves hair cell survival, opening up novel strategies to prevent and treat aminoglycoside ototoxicity.

Publication types

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

MeSH terms

  • Alanine / analogs & derivatives
  • Alkynes
  • Aminoglycosides / metabolism
  • Aminoglycosides / toxicity*
  • Animals
  • Anti-Bacterial Agents / metabolism
  • Anti-Bacterial Agents / toxicity*
  • Apoptosis / drug effects
  • Blotting, Western
  • Cell Count
  • Chick Embryo
  • Cytosol / metabolism*
  • Ear Diseases / chemically induced*
  • Enzyme Activation / drug effects
  • Evoked Potentials, Auditory, Brain Stem / drug effects
  • Glycine / analogs & derivatives
  • Hair Cells, Auditory / drug effects
  • Hair Cells, Auditory / pathology
  • Immunohistochemistry
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Mice
  • Mice, Inbred CBA
  • Niacinamide / analogs & derivatives
  • Niacinamide / pharmacology
  • Organ Culture Techniques
  • Phenylurea Compounds / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Protein Synthesis Inhibitors / metabolism
  • Protein Synthesis Inhibitors / toxicity*
  • RNA, Ribosomal / metabolism
  • Sorafenib

Substances

  • Alkynes
  • Aminoglycosides
  • Anti-Bacterial Agents
  • Phenylurea Compounds
  • Protein Kinase Inhibitors
  • Protein Synthesis Inhibitors
  • RNA, Ribosomal
  • azidohomoalanine
  • homopropargylglycine
  • Niacinamide
  • Sorafenib
  • JNK Mitogen-Activated Protein Kinases
  • Alanine
  • Glycine