Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C

Lauren T. Knapp, Eric Klann

Research output: Contribution to journalArticlepeer-review

Abstract

Recent evidence suggests that reactive oxygen species (ROS), including superoxide, are not only neurotoxic but function as small messenger molecules in normal neuronal processes such as synaptic plasticity. Consistent with this idea, we show that brief incubation of hippocampal slices with the superoxidegenerating system xanthine/xanthine oxidase (X/XO) produces a long-lasting potentiation of synaptic transmission in area CA1. We found that X/XO-induced potentiation was associated with a persistent superoxide-dependent increase in autonomous PKC activity that could be isolated via DEAE column chromatography. The X/XO-induced potentiation was blocked by the inhibition of PKC, indicating that the superoxide-dependent increase in autonomous PKC activity was necessary for the potentiation. We also found that X/XO-induced potentiation and long-term potentiation (LTP) occluded one another, suggesting that these forms of plasticity share similar cellular mechanisms. In further support of this idea, we found that a persistent, superoxide-dependent increase in autonomous PKC activity isolated via DEAE column chromatography also was associated with LTP. Taken together, our findings indicate that X/XO-induced potentiation and LTP share similar cellular mechanisms, including superoxide-dependent increases in autonomous PKC activity. Finally, our findings suggest that superoxide, in addition to its well known role as a neurotoxin, also can be considered a small messenger molecule critical for normal neuronal signaling.

Original languageEnglish (US)
Pages (from-to)674-683
Number of pages10
JournalJournal of Neuroscience
Volume22
Issue number3
DOIs
StatePublished - Feb 1 2002

Keywords

  • Hippocampus
  • Long-term potentiation
  • Protein kinase C
  • Reactive oxygen species
  • Superoxide
  • Synaptic plasticity

ASJC Scopus subject areas

  • Neuroscience(all)

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