Insulin Diminishes Superoxide Increase in Cytosol and Mitochondria of Cultured Cortical Neurons Treated with Toxic Glutamate

Int J Mol Sci. 2022 Oct 20;23(20):12593. doi: 10.3390/ijms232012593.

Abstract

Glutamate excitotoxicity is involved in the pathogenesis of many disorders, including stroke, traumatic brain injury, and Alzheimer's disease, for which central insulin resistance is a comorbid condition. Neurotoxicity of glutamate (Glu) is primarily associated with hyperactivation of the ionotropic N-methyl-D-aspartate receptors (NMDARs), causing a sustained increase in intracellular free calcium concentration ([Ca2+]i) and synchronous mitochondrial depolarization and an increase in intracellular superoxide anion radical (O2-•) production. Recently, we found that insulin protects neurons against excitotoxicity by decreasing the delayed calcium deregulation (DCD). However, the role of insulin in O2-• production in excitotoxicity still needs to be clarified. The present study aims to investigate insulin's effects on glutamate-evoked O2-• generation and DCD using the fluorescent indicators dihydroethidium, MitoSOX Red, and Fura-FF in cortical neurons. We found a linear correlation between [Ca2+]i and [O2-•] in primary cultures of the rat neuron exposed to Glu, with insulin significantly reducing the production of intracellular and mitochondrial O2-• in the primary cultures of the rat neuron. MK 801, an inhibitor of NMDAR-gated Ca2+ influx, completely abrogated the glutamate effects in both the presence and absence of insulin. In experiments in sister cultures, insulin diminished neuronal death and O2 consumption rate (OCR).

Keywords: glutamate (Glu) excitotoxicity; insulin; intracellular free Ca2+ concentration ([Ca2+]i); intracellular superoxide (O2–•); mitochondrial superoxide production; primary cortical neurons.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cells, Cultured
  • Cytosol / metabolism
  • Dizocilpine Maleate / pharmacology
  • Glutamic Acid* / metabolism
  • Insulin / metabolism
  • Mitochondria / metabolism
  • Neurons / metabolism
  • Rats
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Superoxides* / metabolism

Substances

  • Glutamic Acid
  • Superoxides
  • Calcium
  • Dizocilpine Maleate
  • Receptors, N-Methyl-D-Aspartate
  • Insulin