Publication Date

10-1-2021

Journal

Neurobiology of Disease

DOI

10.1016/j.nbd.2021.105470

PMID

34371143

PMCID

PMC8939287

PubMedCentral® Posted Date

10-1-2022

PubMedCentral® Full Text Version

Author MSS

Published Open-Access

yes

Keywords

Animals, Astrocytes, Behavior, Animal, Electroencephalography, Epilepsy, Glial Fibrillary Acidic Protein, Glucose Metabolism Disorders, Mice, Mice, Inbred C57BL, Mice, Knockout, Mitochondria, Motor Activity, Neurons, Oxidative Stress, Primary Cell Culture, Rats, Superoxide Dismutase, Superoxides

Abstract

Mitochondrial superoxide (O2.−) production is implicated in aging, neurodegenerative disease, and most recently epilepsy. Yet the specific contribution of neuronal O2.− to these phenomena is unclear. Here, we selectively deleted superoxide dismutase-2 (SOD2) in neuronal basic helix-loop-helix transcription factor (NEX)-expressing cells restricting deletion to a subset of excitatory principle neurons primarily in the forebrain (cortex and hippocampus). This resulted in nSOD2 KO mice that lived into adulthood (2-3 months) with epilepsy, selective loss of neurons, metabolic rewiring and a marked mitohormetic gene response. Surprisingly, expression of an astrocytic gene, glial fibrillary acidic protein (GFAP) was significantly increased relative to WT. Further studies in rat primary neuron-glial cultures showed that increased mitochondrial O2.−, specifically in neurons, was sufficient to upregulate GFAP. These results suggest that neuron-specific mitochondrial O2.− is sufficient to drive a complex and catastrophic epileptic phenotype and highlights the ability of SOD2 to act in a cell-nonautonomous manner to influence an astrocytic response.

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