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The Journal of Neuroscience, July 28, 2004, 24(30):6842-6852; doi:10.1523/JNEUROSCI.5471-03.2004

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Neurobiology of Disease
Brain-Derived Neurotrophic Factor mRNA and Protein Are Targeted to Discrete Dendritic Laminas by Events That Trigger Epileptogenesis

Enrico Tongiorgi,¹ Mara Armellin,^1,2 Piero Giulio Giulianini,¹ Gianni Bregola,^3,4 Silvia Zucchini,^3,4 Beatrice Paradiso,^3,4 Oswald Steward,⁵ Antonino Cattaneo,² and Michele Simonato^3,4

¹BRAIN Centre for Neuroscience, Department of Biology, University of Trieste, 34127 Trieste, Italy, ²SISSA, International School for Advanced Studies, 34014 Trieste, Italy, ³Department of Clinical and Experimental Medicine, Section of Pharmacology, and ⁴Neuroscience Center, University of Ferrara, 44100 Ferrara, Italy, and ⁵Reeve-Irvine Research Center and Departments of Anatomy and Neurobiology, Neurobiology and Behavior, and Neurosurgery, University of California at Irvine, Irvine, California 92651

Dendritic targeting of mRNA and local protein synthesis are mechanisms that enable neurons to deliver proteins to specific postsynaptic sites. Here, we demonstrate that epileptogenic stimuli induce a dramatic accumulation of BDNF mRNA and protein in the dendrites of hippocampal neurons in vivo. BDNF mRNA and protein accumulate in dendrites in all hippocampal subfields after pilocarpine seizures and in selected subfields after other epileptogenic stimuli (kainate and kindling). BDNF accumulates selectively in discrete dendritic laminas, suggesting targeting to synapses that are active during seizures. Dendritic targeting of BDNF mRNA occurs during the time when the cellular changes that underlie epilepsy are occurring and is not seen after intense stimuli that are non-epileptogenic, including electroconvulsive seizures and high-frequency stimulation. MK801, an NMDA receptor antagonist that can prevent epileptogenesis but not acute seizures, prevents the dendritic accumulation of BDNF mRNA, indicating that dendritic targeting is mediated via NMDA receptor activation. Together, these results suggest that dendritic accumulation of BDNF mRNA and protein play a critical role in the cellular changes leading to epilepsy.

Key words: neurotrophins; rat hippocampus; epilepsy; plasticity; mRNA trafficking; AMPA receptors; NMDA receptors; muscarinic acetylcholine receptors

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Received Dec 12, 2003; revised June 14, 2004; accepted June 14, 2004.

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