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The Journal of Neuroscience, October 20, 2004, 24(42):9324-9331; doi:10.1523/JNEUROSCI.2350-04.2004

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Cellular/Molecular
Persistent Accumulation of Calcium/Calmodulin-Dependent Protein Kinase II in Dendritic Spines after Induction of NMDA Receptor-Dependent Chemical Long-Term Potentiation

Nikolai Otmakhov,¹ Jung-Hwa Tao-Cheng,³ Stephen Carpenter,¹ Brent Asrican,¹ Ayse Dosemeci,⁴ Thomas S. Reese,³ and John Lisman²

¹Department of Biology and ²Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454, ³National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, and ⁴Marine Biological Laboratory, Woods Hole, Massachusetts 02543

Calcium/calmodulin-dependent protein kinase II (CaMKII) is a leading candidate for a synaptic memory molecule because it is persistently activated after long-term potentiation (LTP) induction and because mutations that block this persistent activity prevent LTP and learning. Previous work showed that synaptic stimulation causes a rapidly reversible translocation of CaMKII to the synaptic region. We have now measured green fluorescent protein (GFP)-CaMKII translocation into synaptic spines during NMDA receptor-dependent chemical LTP (cLTP) and find that under these conditions, translocation is persistent. Using red fluorescent protein as a cell morphology marker, we found that there are two components of the persistent accumulation. cLTP produces a persistent increase in spine volume, and some of the increase in GFP-CaMKII is secondary to this volume change. In addition, cLTP results in a dramatic increase in the bound fraction of GFP-CaMKII in spines. To further study the bound pool, immunogold electron microscopy was used to measure CaMKII in the postsynaptic density (PSD), an important regulator of synaptic function. cLTP produced a persistent increase in the PSD-associated pool of CaMKII. These results are consistent with the hypothesis that CaMKII accumulation at synapses is a memory trace of past synaptic activity.

Key words: protein kinase; postsynaptic density; imaging; synapse; LTP; long-term potentiation; EM; tissue culture; fluorescence

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Received Sep 8, 2003; revised August 19, 2004; accepted August 24, 2004.

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