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The Journal of Neuroscience, September 15, 2000, 20(18):6811-6819
The Inhibitory Effect of Interleukin-1 on Long-Term
Potentiation Is Coupled with Increased Activity of
Stress-Activated Protein Kinases
E.
Vereker,
E.
O'Donnell, and
M. A.
Lynch
Department of Physiology, Trinity College, Dublin 2, Ireland
Long-term potentiation (LTP) in perforant path-granule cell
synapses is decreased in aged rats, stressed rats, and rats injected intracerebroventricularly with the proinflammatory cytokine
interleukin-1 (IL-1). One factor that is common to these
experimental conditions is an increase in the concentration of IL-1
in the dentate gyrus, suggesting a causal relationship between the
compromise in LTP and increased IL-1 concentration. In this study,
we have investigated the downstream consequences of an increase in
IL-1 concentration and report that the reduced LTP in rats injected
intracerebroventricularly with IL-1 was accompanied by a decrease in
KCl-stimulated glutamate release in synaptosomes prepared from dentate
gyrus, although unstimulated glutamate release was increased. These
changes were paralleled by increased activity of the stress-activated
kinases, c-Jun N-terminal kinase (JNK) and p38 mitogen-activated
protein kinase. Intracerebroventricular injection of IL-1
increased reactive oxygen species production in hippocampal tissue,
whereas IL-1 and H2O2 increased activities
of both JNK and p38 in vitro. Dietary manipulation with
antioxidant vitamins E and C blocked the increase in reactive oxygen
species production, the stimulation of JNK and p38 activity, the
attenuation of glutamate release, and the IL-1-induced inhibitory of
LTP. We propose that IL-1 stimulates activity of stress-activated
kinases, which in turn may inhibit glutamate release and result in
compromised LTP and that these actions are a consequence of increased
production of reactive oxygen species.
Key words:
LTP; dentate gyrus; IL-1; stress-activated kinases; glutamate release; reactive oxygen species
Copyright © 2000 Society for Neuroscience 0270-6474/00/20186811-09$05.00/0
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