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The Journal of Neuroscience, December 1, 1999, 19(23):10250-10261
Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB
Phosphorylation in the Hippocampus
Yun-Fei
Lu1,
Eric R.
Kandel1, 2, 3, and
Robert D.
Hawkins1, 2
1 Center for Neurobiology and Behavior, College of
Physicians and Surgeons, Columbia University, 2 New York
State Psychiatric Institute, and 3 Howard Hughes Medical
Institute, New York, New York 10032
Long-term potentiation (LTP) in the hippocampus has an early phase
(E-LTP) that can be induced by one- or two-train tetanization, lasts ~1 hr, and is cAMP-dependent protein kinase (PKA) and protein synthesis independent and a late phase (L-LTP) that can be induced by
three- or four-train tetanization, lasts >3 hr, and is reduced by
inhibitors of PKA and of protein or RNA synthesis. Nitric oxide (NO) is
thought to be involved in E-LTP, but until now there has been no
information about the role of the NO-signaling pathway in L-LTP. We
examined this question at the Schaffer collateral-CA1 synapses in
slices of mouse hippocampus. An inhibitor of NO synthase blocked L-LTP
induced by three-train tetanization and reduced L-LTP induced by
four-train tetanization, whereas an inhibitor of PKA was more effective
in blocking four-train L-LTP than three-train L-LTP. Three-train L-LTP
was also blocked by inhibitors of guanylyl cyclase or cGMP-dependent
protein kinase (PKG). Conversely, either NO or cGMP analogs paired with
one-train tetanization produced late-phase potentiation, and the
cGMP-induced potentiation was blocked by inhibitors of protein or RNA
synthesis and an inhibitor of PKG, but not by an inhibitor of PKA. To
test a possible downstream target of PKG, we examined changes in
phospho-CRE-binding protein (phospho-CREB) immunofluorescence in the
CA1 cell body area and obtained results similar to those of the
electrophysiology experiments. These results suggest that NO
contributes to L-LTP by stimulating guanylyl cyclase and cGMP-dependent
protein kinase, which acts in parallel with PKA to increase
phosphorylation of the transcription factor CREB.
Key words:
nitric oxide; guanylyl cyclase; cGMP-dependent protein
kinase; long-term potentiation; CREB; hippocampus
Copyright © 1999 Society for Neuroscience 0270-6474/99/192310250-12$05.00/0
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