Characterization of Ca2+ signalling in postnatal mouse retinal ganglion cells: involvement of OPA1 in Ca2+ clearance

Ophthalmic Genet. 2010 Jun;31(2):53-65. doi: 10.3109/13816811003698117.

Abstract

Purpose: The regulation of Ca(2+) entry and removal is a fine-tuned process which remains not well understood in mouse retinal ganglion cells (RGCs). The latter are known to be sensitive to dysfunctions of mitochondria, organelles playing a pivotal role in Ca(2+) reuptake.

Methods: We first described the Ca(2+) signals of RGCs in response to varied drugs with Fura-2 imaging, and secondly tested the role of optic atrophy 1 or OPA1, the gene responsible for Autosomal Dominant Optic Atrophy, on mitochondrial ability to capture intracellular Ca(2+) in cells transfected with the OPA1 small interfering ribonucleic acids (siRNAs).

Results: In control RGCs, K(+)-evoked [Ca(2+)](i) increase was blocked by the Ca(2+) channel antagonists (Ni(2+)+ Cd(2+)) and GABA(A) receptor agonist muscimol-induced [Ca(2+)](i) responses were attenuated by the GABA(A) receptor antagonists, picrotoxin and gabazine. We also prove the presence of NMDA and AMPA/Kainate (glutamate receptor agonists) responsive receptors in this model. Application of cyclopiazonic acid, an inhibitor of Ca(2+)-ATPase pumps of the intracellular Ca(2+) stores, induced an increase in [Ca(2+)](i) while ryanodine or caffeine had no effect on resting [Ca(2+)](i). Spontaneous Ca(2+) oscillations in contacting neurons highlighted the importance of cross-talks between RGCs during maturation. The mitochondrial respiration uncoupler, carbonyl cyanide 3-chlorophenylhydrazone (CCCP), induced robust raises of intracellular Ca(2+) after K(+) application, with a more pronounced effect in cells silenced for OPA1, which could lead to cell death.

Conclusions: Our results indicate an important role of OPA1 in mitochondrial dependent Ca(2+) homeostasis and cell survival in RGCs, suggesting a possible patho-physiological mechanism involved in inherited optic neuropathies.

MeSH terms

  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Calcium Signaling / physiology*
  • Calcium-Transporting ATPases / antagonists & inhibitors
  • Calcium-Transporting ATPases / metabolism
  • Cell Survival
  • Cells, Cultured
  • Cytosol / metabolism
  • Fura-2 / metabolism
  • GABA-A Receptor Antagonists
  • GTP Phosphohydrolases / physiology*
  • Homeostasis
  • Indoles / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Confocal
  • Mitochondria / metabolism
  • Potassium / pharmacology
  • RNA, Small Interfering / genetics
  • Receptors, AMPA / metabolism
  • Receptors, GABA-A / metabolism
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Retinal Ganglion Cells / drug effects
  • Retinal Ganglion Cells / metabolism*
  • Transfection

Substances

  • Calcium Channel Blockers
  • GABA-A Receptor Antagonists
  • Indoles
  • RNA, Small Interfering
  • Receptors, AMPA
  • Receptors, GABA-A
  • Receptors, N-Methyl-D-Aspartate
  • GTP Phosphohydrolases
  • Opa1 protein, mouse
  • Calcium-Transporting ATPases
  • Potassium
  • Calcium
  • Fura-2
  • cyclopiazonic acid