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First published online April 1, 2009
doi: 10.1242/10.1242/jcs.043729

Journal of Cell Science 122, 1211-1219 (2009)
Published by The Company of Biologists 2009
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Research Article

Activity of the AMPA receptor regulates drebrin stabilization in dendritic spine morphogenesis

Hideto Takahashi1,2,*, Hiroyuki Yamazaki1, Kenji Hanamura1, Yuko Sekino1,3,4 and Tomoaki Shirao1,{ddagger}

1 Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan
2 ERCGSM, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan
3 CREST, JST, Kawaguchi, Saitama, 332-0012, Japan
4 Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo, 1108-8639, Japan

{ddagger} Author for correspondence (e-mail: tshirao{at}med.gunma-u.ac.jp)

Accepted 15 December 2008

Spine morphogenesis mainly occurs during development as a morphological shift from filopodia-like thin protrusions to bulbous ones. We have previously reported that synaptic clustering of the actin-binding protein drebrin in dendritic filopodia governs spine morphogenesis and synaptic PSD-95 clustering. Here, we report the activity-dependent cellular mechanisms for spine morphogenesis, in which the activity of AMPA receptors (AMPARs) regulates drebrin clustering in spines by promoting drebrin stabilization. In cultured developing hippocampal neurons, pharmacological blockade of AMPARs, but not of other glutamate receptors, suppressed postsynaptic drebrin clustering without affecting presynaptic clustering of synapsin I (synapsin-1). Conversely, the enhancement of the action of AMPARs promoted drebrin clustering in spines. When we explored drebrin dynamics by photobleaching individual spines, we found that AMPAR activity increased the fraction of stable drebrin without affecting the time constant of drebrin turnover. An increase in the fraction of stable drebrin corresponded with increased drebrin clustering. AMPAR blockade also suppressed normal morphological maturation of spines and synaptic PSD-95 clustering in spines. Together, these data suggest that AMPAR-mediated stabilization of drebrin in spines is an activity-dependent cellular mechanism for spine morphogenesis.

Key words: Dendritic spine, AMPA receptor, Drebrin, Actin cytoskeleton, Synapse development, Synaptic plasticity


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