Synaptopodin regulates release of calcium from stores in dendritic spines of cultured hippocampal neurons

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Abstract

Non–technical summary

Dendritic spines of central neurons contain calcium stores, but their involvement in synaptic plasticity is not entirely clear. Synaptopodin, an actin–binding molecule, has been localized in the neck of some dendritic spines, and assumed to play a role in regulation of calcium stores in the spines. In the present study we used flash photolysis of calcium inside dendritic spines of cultured hippocampal neurons loaded with the calcium sensor Fluo–4. An ultrafast UV flash generated a rapid rise in [Ca2+]i followed by a monoexponential decay back to control level. In spines where synaptopodin was found in post hoc immunocytochemical analysis, the decay of elevated calcium was much prolonged compared to synaptopodin–negative spines. This prolongation was eliminated by blockade of release of calcium from stores. Our results provide the first direct demonstration of calcium release from stores in dendritic spines of central neurons.

The presence of calcium stores and their function in dendritic spines is still unsettled. We have now studied the kinetics of calcium released inside dendritic spines of cultured rat hippocampal neurons by flash photolysis of caged calcium. Photolysis of calcium produced a fast rise in [Ca2+]i, followed by a variable decay. We were able to correlate the decay of elevated [Ca2+]i with the presence of synaptopodin (SP), an actin–binding protein, in the spines; spines containing SP generated the same initial [Ca2+]i transient, but their decay time was significantly slower and more complex than that of SP–negative ones. The altered decay kinetics of the flash–elevated [Ca2+]i transient was blocked by thapsigargin or cyclopiazonic acid (CPA), indicating that this kinetic change is due to compartmentalized release of calcium from intracellular stores. Thus, SP plays a pivotal role in the calcium store–associated ability of spines to locally tune calcium kinetics.

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