Interleukin-1 beta protects neurons via the interleukin-1 (IL-1) receptor-mediated Akt pathway and by IL-1 receptor-independent decrease of transmembrane currents in vivo

Mol Cell Neurosci. 2003 Apr;22(4):487-500. doi: 10.1016/s1044-7431(02)00042-8.

Abstract

Recently, we have demonstrated that tumor necrosis factor-alpha (TNF-alpha) rescues retinal ganglion cells (RGCs) from retrograde cell death in vivo after axotomy of the optic nerve. The mechanism of RGC rescue was dependent on TNF-receptor I-mediated potassium current reduction and consecutive activation of the phosphatidylinositol 3-kinase (PI3-K)/Akt pathway. Here, we present evidence that interleukin-1 beta (IL-1 beta) also promotes RGC survival, but shows distinct differences with respect to its neuroprotective mechanisms. Using whole-cell and outside-out patch-clamp techniques, we observed that IL-1 beta decreased both inward sodium current amplitudes and outward potassium current amplitudes. Counteracting these effects by sodium or potassium channel opening inhibited the survival-promoting effects of this cytokine. IL-1 beta-induced current reduction could not be abolished by the interleukin-1 receptor antagonist, indicating that the electrophysiological effects of IL-1 beta are independent of interleukin-1 receptor I (IL-1RI) activation. Western blot analysis revealed an IL-1 beta-induced IL-1RI-dependent upregulation of phospho-Akt. Antagonism of the survival-promoting effects of IL-1 beta by PI3-K inhibition revealed the functional relevance of the PI3-K/Akt pathway in IL-1 beta-induced signal transduction in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axotomy
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Survival / drug effects
  • Cell Survival / physiology*
  • Cells, Cultured
  • Enzyme Inhibitors / pharmacology
  • Female
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1 / metabolism*
  • Interleukin-1 / pharmacology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Nerve Degeneration / metabolism*
  • Nerve Degeneration / physiopathology
  • Neuroprotective Agents / metabolism*
  • Neuroprotective Agents / pharmacology
  • Optic Nerve / surgery
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Potassium Channels / drug effects
  • Potassium Channels / metabolism*
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / drug effects
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Interleukin-1 / drug effects
  • Receptors, Interleukin-1 / metabolism
  • Receptors, Interleukin-1 Type I
  • Retinal Ganglion Cells / cytology
  • Retinal Ganglion Cells / drug effects
  • Retinal Ganglion Cells / metabolism*
  • Sialoglycoproteins / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Sodium Channels / drug effects
  • Sodium Channels / metabolism*

Substances

  • Enzyme Inhibitors
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1
  • Neuroprotective Agents
  • Phosphoinositide-3 Kinase Inhibitors
  • Potassium Channels
  • Proto-Oncogene Proteins
  • Receptors, Interleukin-1
  • Receptors, Interleukin-1 Type I
  • Sialoglycoproteins
  • Sodium Channels
  • Akt1 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt