ER-mitochondrial calcium flow underlies vulnerability of mechanosensory hair cells to damage

J Neurosci. 2014 Jul 16;34(29):9703-19. doi: 10.1523/JNEUROSCI.0281-14.2014.

Abstract

Mechanosensory hair cells are vulnerable to environmental insult, resulting in hearing and balance disorders. We demonstrate that directional compartmental flow of intracellular Ca(2+) underlies death in zebrafish lateral line hair cells after exposure to aminoglycoside antibiotics, a well characterized hair cell toxin. Ca(2+) is mobilized from the ER and transferred to mitochondria via IP3 channels with little cytoplasmic leakage. Pharmacological agents that shunt ER-derived Ca(2+) directly to cytoplasm mitigate toxicity, indicating that high cytoplasmic Ca(2+) levels alone are not cytotoxic. Inhibition of the mitochondrial transition pore sensitizes hair cells to the toxic effects of aminoglycosides, contrasting with current models of excitotoxicity. Hair cells display efficient ER-mitochondrial Ca(2+) flow, suggesting that tight coupling of these organelles drives mitochondrial activity under physiological conditions at the cost of increased susceptibility to toxins.

Keywords: lateral line; zebrafish.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aminoglycosides / pharmacology
  • Animals
  • Animals, Genetically Modified
  • Calcium / metabolism*
  • Cell Death / drug effects
  • Chelating Agents / pharmacology
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism
  • Dose-Response Relationship, Drug
  • Egtazic Acid / pharmacology
  • Embryo, Nonmammalian
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / genetics
  • Endoplasmic Reticulum / metabolism*
  • Larva
  • Lateral Line System / anatomy & histology
  • Mechanoreceptors / drug effects
  • Mechanoreceptors / metabolism*
  • Membrane Potential, Mitochondrial / drug effects
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Myosin Heavy Chains / genetics
  • Time Factors
  • Transcription Factor Brn-3C / genetics
  • Zebrafish

Substances

  • Aminoglycosides
  • Chelating Agents
  • Transcription Factor Brn-3C
  • myosin VI
  • Egtazic Acid
  • Myosin Heavy Chains
  • Calcium