IGF-1 alleviates NMDA-induced excitotoxicity in cultured hippocampal neurons against autophagy via the NR2B/PI3K-AKT-mTOR pathway

J Cell Physiol. 2014 Nov;229(11):1618-29. doi: 10.1002/jcp.24607.

Abstract

Insulin-like growth factor-1 (IGF-1) is a brain-specific multifunctional protein involved in neuronal polarity and axonal guidance. Mature IGF-1 triggers three enzymes, mitogen-activated protein kinase (MAPK), phosphatidylinositol 3-kinase (PI3K), and phosphoinositide phospholipase C-γ (PLC-γ), which are its predominant downstream regulators. The PI3K-AKT signaling pathway is upstream of the mammalian target of rapamycin (mTOR), which is of great importance in the induction of autophagy. However, whether the neuroprotective effect of IGF-1 against excitotoxicity is mediated by autophagy through the PI3K/AKT/mTOR pathway remains to be elucidated. The induction of autophagy following NMDA treatment was determined by microtubule-associated protein light chain 3 (LC3) conversion and the result of this autophagy was assessed by monitoring the cleavage of caspase 3 in cultured hippocampal neurons. Cell viability was determined using MTT and LDH assay, and PI-staining was used to estimate the fate of autophagy and the protective effect of IGF-1. In addition, IGF-1 was found to decrease autophagy induced by NMDA using transmission electron microscopy and MDC staining. The protective effect of IGF-1 against autophagy was accompanied with up-regulation of phospho-AKT (p-AKT) and phospho-mTOR (p-mTOR), which was blocked by the inhibitor of PI3K. At the same time, the activation of NR2B resulting in the down-regulation of p-AKT and p-mTOR was blocked by IGF-1. Together, these data suggest that NMDA induces the autophagy, followed by apoptosis in cultured hippocampal neurons, and that IGF-1 can block this effect via inhibition of NR2B receptors and activation of the PI3K-AKT-mTOR pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / metabolism
  • Autophagy / drug effects*
  • Beclin-1
  • Caspase 3 / metabolism
  • Cells, Cultured
  • Excitatory Postsynaptic Potentials / drug effects
  • Female
  • Hippocampus / pathology*
  • Insulin-Like Growth Factor I / pharmacology*
  • Microtubule-Associated Proteins / metabolism
  • Models, Biological
  • N-Methylaspartate / toxicity*
  • Neurons / drug effects
  • Neurons / enzymology
  • Neurons / pathology*
  • Neurons / ultrastructure
  • Neurotoxins / toxicity*
  • Phagosomes / drug effects
  • Phagosomes / metabolism
  • Phagosomes / ultrastructure
  • Phosphatidylinositol 3-Kinase / metabolism
  • Phosphorylation / drug effects
  • Phosphoserine / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Signal Transduction / drug effects*
  • Synapses / drug effects
  • Synapses / metabolism
  • Synapses / ultrastructure
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • Beclin-1
  • Becn1 protein, rat
  • LC3 protein, rat
  • Microtubule-Associated Proteins
  • NR2B NMDA receptor
  • Neurotoxins
  • Receptors, N-Methyl-D-Aspartate
  • Phosphoserine
  • N-Methylaspartate
  • Insulin-Like Growth Factor I
  • Phosphatidylinositol 3-Kinase
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Caspase 3