Inflammatory cytokines disrupt astrocyte exosomal HepaCAM-mediated protection against neuronal excitotoxicity in the SOD1G93A ALS model

Sci Adv. 2024 Nov 29;10(48):eadq3350. doi: 10.1126/sciadv.adq3350. Epub 2024 Nov 27.

Abstract

Astrocyte secreted signals substantially affect disease pathology in neurodegenerative diseases. It remains little understood about how proinflammatory cytokines, such as interleukin-1α/tumor necrosis factor-α/C1q (ITC), often elevated in neurodegenerative diseases, alter astrocyte-secreted signals and their effects in disease pathogenesis. By selectively isolating astrocyte exosomes (A-Exo.) and employing cell type-specific exosome reporter mice, our current study showed that ITC cytokines significantly reduced A-Exo. secretion and decreased spreading of focally labeled A-Exo. in diseased SOD1G93A mice. Our results also found that A-Exo. were minimally associated with misfolded SOD1 and elicited no toxicity to mouse spinal and human iPSC-derived motor neurons. In contrast, A-Exo. were neuroprotective against excitotoxicity, which was completely diminished by ITC cytokines and partially abolished by SOD1G93A expression. Subsequent proteomic characterization of A-Exo. and genetic analysis identified that surface expression of glial-specific HepaCAM preferentially mediates A-Exo's axon protection effect. Together, our study defines a cytokine-induced loss-of-function mechanism of A-Exo. in protecting neurons from excitotoxicity in amyotrophic lateral sclerosis.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / metabolism
  • Amyotrophic Lateral Sclerosis* / pathology
  • Animals
  • Astrocytes* / metabolism
  • Cytokines* / metabolism
  • Disease Models, Animal*
  • Exosomes* / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Mice
  • Mice, Transgenic*
  • Motor Neurons* / metabolism
  • Motor Neurons* / pathology
  • Neurons / metabolism
  • Superoxide Dismutase-1* / genetics
  • Superoxide Dismutase-1* / metabolism

Substances

  • Cytokines
  • Superoxide Dismutase-1