Caspase inhibitors protect neurons by enabling selective necroptosis of inflamed microglia

J Biol Chem. 2013 Mar 29;288(13):9145-52. doi: 10.1074/jbc.M112.427880. Epub 2013 Feb 5.

Abstract

Microglia are resident brain macrophages, which can cause neuronal loss when activated in infectious, ischemic, traumatic, and neurodegenerative diseases. Caspase-8 has both prodeath and prosurvival roles, mediating apoptosis and/or preventing RIPK1-mediated necroptosis depending on cell type and stimulus. We found that inflammatory stimuli (LPS, lipoteichoic acid, or TNF-α) caused an increase in caspase-8 IETDase activity in primary rat microglia without inducing apoptosis. Inhibition of caspase-8 with either Z-VAD-fmk or IETD-fmk resulted in necrosis of activated microglia. Inhibition of caspases with Z-VAD-fmk did not kill non-activated microglia, or astrocytes and neurons in any condition. Necrostatin-1, a specific inhibitor of RIPK1, prevented microglial caspase inhibition-induced death, indicating death was by necroptosis. In mixed cerebellar cultures of primary neurons, astrocytes, and microglia, LPS induced neuronal loss that was prevented by inhibition of caspase-8 (resulting in microglial necroptosis), and neuronal death was restored by rescue of microglia with necrostatin-1. We conclude that the activation of caspase-8 in inflamed microglia prevents their death by necroptosis, and thus, caspase-8 inhibitors may protect neurons in the inflamed brain by selectively killing activated microglia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis*
  • Caspase 8 / chemistry*
  • Caspase Inhibitors / pharmacology*
  • Cell Survival
  • Cells, Cultured
  • Imidazoles / metabolism
  • Indoles / metabolism
  • Inflammation
  • Lipopolysaccharides / metabolism
  • Microglia / metabolism*
  • Models, Biological
  • Necrosis*
  • Neuroglia / metabolism
  • Neurons / metabolism
  • Rats
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Caspase Inhibitors
  • Imidazoles
  • Indoles
  • Lipopolysaccharides
  • Tumor Necrosis Factor-alpha
  • necrostatin-1
  • RIPK1 protein, human
  • Receptor-Interacting Protein Serine-Threonine Kinases
  • Caspase 8