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The Journal of Neuroscience, July 19, 2006, 26(29):7693-7706; doi:10.1523/JNEUROSCI.0522-06.2006

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Cellular/Molecular
Differential Control of Postsynaptic Density Scaffolds via Actin-Dependent and -Independent Mechanisms

Toshihiko Kuriu,^1,2,3,6 Akihiro Inoue,¹ Haruhiko Bito,^4,6 Kenji Sobue,⁵ and Shigeo Okabe^1,2,3,6

¹Department of Cell Biology, School of Medicine, and ²COE Program for Brain Integration and its Disorders, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8519, Japan, ³Molecular Neurophysiology Group, Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 305-8566, Japan, ⁴Department of Neurochemistry, University of Tokyo Graduate School of Medicine, Bunkyo-ku, Tokyo 113-0033, Japan, ⁵Department of Neuroscience (D13), Osaka University Graduate School of Medicine, Suita, Osaka 565-0871, Japan, and ⁶Solution Oriented Research for Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Correspondence should be addressed to Dr. Shigeo Okabe, Department of Cell Biology, School of Medicine, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. Email: okabe.cbio{at}tmd.ac.jp

Organization and dynamic remodeling of postsynaptic density (PSD) are thought to be critical in postsynaptic signal transduction, but the underlying molecular mechanisms are not well understood. We show here that four major scaffolding molecules, PSD-95, GKAP, Shank, and PSD-Zip45, show distinct instability in total molecular content per synapse. Fluorescence recovery after photobleaching also confirmed their distinct turnover rates. Among the PSD molecules examined, PSD-95 was most stable, but its elimination did not influence the dynamics of its direct binding partner GKAP. Multiple interactions of scaffolding molecules with the actin cytoskeleton have suggested their importance in both maintenance and remodeling of the PSD. Indeed, acute pharmacological disruption of F-actin rapidly eliminated the dynamic fraction of GKAP, Shank, and PSD-Zip45, without changing synaptic localization of PSD-95. GKAP content in synapses increased after pharmacological enhancement of neuronal activity, whereas Shank and PSD-Zip45 content showed reduction. Inhibition of F-actin dynamics prevented activity-dependent redistribution of all three scaffolds. We also assessed involvement of glutamate receptors in the regulation of PSD dynamics. Genetic manipulations eliminating either NMDA receptors or metabotropic glutamate receptors did not primarily influence mobility of their binding scaffolds. These results collectively indicate a critical role of filamentous actin in determining the extent of dynamic reorganization in PSD molecular composition.

Key words: postsynaptic density; actin cytoskeleton; synaptic plasticity; green fluorescent protein (GFP); hippocampus; time-lapse imaging

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Received June 25, 2005; revised June 2, 2006; accepted June 13, 2006.

Correspondence should be addressed to Dr. Shigeo Okabe, Department of Cell Biology, School of Medicine, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. Email: okabe.cbio{at}tmd.ac.jp

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