Cell death in amyotrophic lateral sclerosis: interplay between neuronal and glial cells

FASEB J. 2004 Aug;18(11):1261-3. doi: 10.1096/fj.03-1199fje. Epub 2004 Jun 18.

Abstract

Mutations in the gene coding for the ubiquitous, anti-oxidant enzyme Cu,Zn superoxide dismutase (SOD1) are associated with familial amyotrophic lateral sclerosis (fALS), a fatal disease characterized by selective loss of motor neurons. Expression of a mutant SOD1 typical of fALS patients restricted to either motor neurons or astrocytes is insufficient to generate a pathological phenotype in mouse models, suggesting that a deleterious interplay between different cell types is necessary for the pathogenesis of the disease. In this study, we demonstrate the actual role of a functional cross-talk between glial and neuronal cells expressing fALS mutant G93A-SOD1, where an increase in the production of reactive oxygen species occurs. We show that human glioblastoma cells expressing G93A-SOD1 induce activation of caspase-1, release of cytokines, and activation of apoptotic pathways in cocultured human neuroblastoma cells also expressing G93A-SOD1. Activation of caspase-1 and caspase-3 is observed also in neuroblastoma lines expressing other fALS-SOD1s (G37R, G85R, and I113T) cocultured with glioblastoma lines expressing the corresponding mutant enzymes. These effects are consequent to activation of inflammatory processes in G93A-glioblastoma cells stimulated by cocultured G93A-neuroblastoma. Furthermore, selective death of embryonal spinal motor neurons from G93A-SOD1 transgenic mice is induced by coculture with G93A-glioblastoma and prevented by inhibition of NO synthase. Proinflammatory cytokines, interferon-gamma, and nitric oxide are among the molecular signals exchanged between glial and neuronal cells that generate a functional interplay between the two cell types. This cross-talk may be crucial for the pathogenesis of SOD1-linked fALS but also for the more common sporadic form of the disease, where markers of increased oxidative stress and of glial activation have been found.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Caspase 1 / metabolism
  • Catalase / analysis
  • Cell Communication / physiology*
  • Coculture Techniques
  • Cytokines / metabolism
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Glioblastoma / pathology
  • Humans
  • Interferon-gamma / pharmacology
  • Lipopolysaccharides / pharmacology
  • Mice
  • Mice, Transgenic
  • Motor Neuron Disease / pathology*
  • Motor Neurons / pathology
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Neuroblastoma / pathology
  • Neuroglia / pathology*
  • Neurons / pathology*
  • Nitric Oxide Donors / pharmacology
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitroso Compounds / pharmacology
  • Oxidative Stress
  • Reactive Oxygen Species
  • Spinal Cord / cytology
  • Spinal Cord / embryology
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / physiology*
  • Superoxide Dismutase-1
  • Transfection

Substances

  • Cytokines
  • Enzyme Inhibitors
  • Lipopolysaccharides
  • NOC 18
  • Nitric Oxide Donors
  • Nitroso Compounds
  • Reactive Oxygen Species
  • SOD1 protein, human
  • Interferon-gamma
  • Catalase
  • Nitric Oxide Synthase
  • SOD1 G93A protein
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Caspase 1
  • NG-Nitroarginine Methyl Ester