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

Lauren T. Knapp, Eric Klann

Research output: Contribution to journalArticle

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
StatePublished - Feb 1 2002

Fingerprint

Xanthine
Xanthine Oxidase
Synaptic Transmission
Superoxides
Protein Kinase C
Long-Term Potentiation
Chromatography
Neuronal Plasticity
Neurotoxins
Reactive Oxygen Species

Keywords

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

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. / Knapp, Lauren T.; Klann, Eric.

In: Journal of Neuroscience, Vol. 22, No. 3, 01.02.2002, p. 674-683.

Research output: Contribution to journalArticle

@article{d3aa8ef96a8c4df2aa7489b49a1af26d,
title = "Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C",
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.",
keywords = "Hippocampus, Long-term potentiation, Protein kinase C, Reactive oxygen species, Superoxide, Synaptic plasticity",
author = "Knapp, {Lauren T.} and Eric Klann",
year = "2002",
month = "2",
day = "1",
language = "English (US)",
volume = "22",
pages = "674--683",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "3",

}

TY - JOUR

T1 - Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C

AU - Knapp, Lauren T.

AU - Klann, Eric

PY - 2002/2/1

Y1 - 2002/2/1

N2 - 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.

AB - 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.

KW - Hippocampus

KW - Long-term potentiation

KW - Protein kinase C

KW - Reactive oxygen species

KW - Superoxide

KW - Synaptic plasticity

UR - http://www.scopus.com/inward/record.url?scp=0036470423&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0036470423&partnerID=8YFLogxK

M3 - Article

VL - 22

SP - 674

EP - 683

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 3

ER -