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The Journal of Neuroscience, August 13, 2003, 23(19):7317-7325

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p38 MAP Kinase Mediates Both Short-Term and Long-Term Synaptic Depression in Aplysia

Zhonghui Guan,1 Joung-Hun Kim,4 Stavros Lomvardas,2 Kerri Holick,1,3 Shiqin Xu,1 Eric R. Kandel,1,2,4 and James H. Schwartz1,2

1Center for Neurobiology and Behavior and 2Departments of Biochemistry and Molecular Biophysics and 3Pharmacology, College of Physicians and Surgeons, Columbia University, New York, New York 10032, and 4Howard Hughes Medical Institute, New York, New York 10032

At Aplysia sensory-to-motor neuron synapses, the inhibitory neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFa) produces depression, and serotonin (5-HT) produces facilitation. Short-term depression has been found to result from the activation of a phospholipase A2. The released arachidonate is metabolized by 12-lipoxygenase to active second messengers. We find that FMRFa leads to the phosphorylation and activation of p38 mitogen-activated protein (MAP) kinase. Short-term depression and the release of arachidonate are blocked by the specific p38 kinase inhibitor SB 203580. Both the inhibitor and an affinity-purified antibody raised against recombinant Aplysia p38 kinase injected into sensory neurons prevented long-term depression, which depends on the phosphorylation of translation factors cAMP response element-binding protein 2 (CREB2) and activating transcription factor 2. Facilitation produced by 5-HT, on the other hand, inactivates p38 kinase. Chromatin immunoprecipitation assays indicate that p38 kinase activates CREB2. p38 kinase also is pivotal in the bidirectional regulation of synaptic plasticity: when the kinase is inhibited, brief treatment with 5-HT that normally produces only short-term facilitation now results in long-term facilitation. Conversely, in sensory neurons injected with the activated kinase, long-term facilitation is blocked, and brief exposure to FMRFa, which normally results in short-term depression, results in long-term depression. We conclude that p38 kinase, which itself is bidirectionally regulated by FMRFa and 5-HT, acts as a modulator of synaptic plasticity by positively regulating depression and serving as an inhibitory constraint for facilitation.

Key words: Aplysia; histone deacetylase; long-term depression; long-term facilitation; phospholipase A2; p38 MAP kinase

Received Oct. 29, 2002; revised Jun. 25, 2003; accepted Jun. 26, 2003.




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