Superoxide-induced potentiation in the hippocampus requires activation of ryanodine receptor type 3 and ERK

A. Tara Huddleston, Wei Tang, Hiroshi Takeshima, Susan L. Hamilton, Eric Klann

Research output: Contribution to journalArticle

Abstract

Reactive oxygen species (ROS) are required for the induction of long-term potentiation (LTP) and behave as signaling molecules via redox modifications of target proteins. In particular, superoxide is necessary for induction of LTP, and application of superoxide to hippocampal slices is sufficient to induce LTP in area CA1. Although a rise in postsynaptic intracellular calcium is necessary for LTP induction, superoxide-induced potentiation does not require calcium flux through N-methyl-D-aspartate (NMDA) receptors. Ryanodine receptors (RyRs) mediate calcium-induced calcium release from intracellular stores and have been shown to modulate LTP. In this study, we investigated the highly redox-sensitive RyRs and L-type calcium channels as calcium sources that might mediate superoxide-induced potentiation. In agreement with previous studies of skeletal and cardiac muscle, we found that superoxide enhances activation of RyRs in the mouse hippocampus. We identified a functional coupling between L-type voltage-gated calcium channels and RyRs and identified RyR3, a subtype enriched in area CA1, as the specific isoform required for superoxide-induced potentiation. Superoxide also enhanced the phosphorylation of extracellular signal-regulated kinase (ERK) in area CA1, and ERK was necessary for superoxide-induced potentiation. Thus superoxide-induced potentiation requires the redox targeting of RyR3 and the subsequent activation of ERK.

Original languageEnglish (US)
Pages (from-to)1565-1571
Number of pages7
JournalJournal of Neurophysiology
Volume99
Issue number3
DOIs
StatePublished - Mar 2008

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Ryanodine Receptor Calcium Release Channel
Extracellular Signal-Regulated MAP Kinases
Superoxides
Hippocampus
Long-Term Potentiation
Calcium
Oxidation-Reduction
Calcium-Sensing Receptors
L-Type Calcium Channels
Calcium Channels
N-Methyl-D-Aspartate Receptors
Reactive Oxygen Species
Myocardium
Protein Isoforms
Skeletal Muscle
Phosphorylation

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Superoxide-induced potentiation in the hippocampus requires activation of ryanodine receptor type 3 and ERK. / Huddleston, A. Tara; Tang, Wei; Takeshima, Hiroshi; Hamilton, Susan L.; Klann, Eric.

In: Journal of Neurophysiology, Vol. 99, No. 3, 03.2008, p. 1565-1571.

Research output: Contribution to journalArticle

Huddleston, A. Tara ; Tang, Wei ; Takeshima, Hiroshi ; Hamilton, Susan L. ; Klann, Eric. / Superoxide-induced potentiation in the hippocampus requires activation of ryanodine receptor type 3 and ERK. In: Journal of Neurophysiology. 2008 ; Vol. 99, No. 3. pp. 1565-1571.
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