Calcium-triggered exit of F-actin and IP3 3-kinase A from dendritic spines is rapid and reversible

Michael J. Schell, Robin F. Irvine

Research output: Contribution to journalArticle

Abstract

The structure of the actin cytoskeleton in dendritic spines is thought to underlie some forms of synaptic plasticity. We have used fixed and live-cell imaging in rat primary hippocampal cultures to characterize the synaptic dynamics of the F-actin binding protein inositol trisphosphate 3-kinase A (IP3K), which is localized in the spines of pyramidal neurons derived from the CA1 region. IP3K was intensely concentrated as puncta in spine heads when Ca2+ influx was low, but rapidly and reversibly redistributed to a striated morphology in the main dendrite when Ca2+ influx was high. Glutamate stimulated the exit of IP3K from spines within 10 s, and re-entry following blockage of Ca2+ influx commenced within a minute; IP3K appeared to remain associated with F-actin throughout this process. Ca 2+-triggered F-actin relocalization occurred in about 90% of the cells expressing IP3K endogenously, and was modulated by the synaptic activity of the cultures, suggesting that it is a physiological process. F-actin relocalization was blocked by cytochalasins, jasplakinolide and by the over-expression of actin fused to green fluorescent protein. We also used deconvolution microscopy to visualize the relationship between F-actin and endoplasmic reticulum inside dendritic spines, revealing a delicate microorganization of IP3K near the Ca2+ stores. We conclude that Ca2+ influx into the spines of CA1 pyramidal neurons triggers the rapid and reversible retraction of F-actin from the dendritic spine head. This process contributes to changes in spine F-actin shape and content during synaptic activity, and might also regulate spine IP3 signals.

Original languageEnglish (US)
Pages (from-to)2491-2503
Number of pages13
JournalEuropean Journal of Neuroscience
Volume24
Issue number9
DOIs
StatePublished - Nov 2006
Externally publishedYes

Fingerprint

Dendritic Spines
Actins
Phosphotransferases
Spine
Calcium
jasplakinolide
Pyramidal Cells
Cytochalasins
Physiological Phenomena
Neuronal Plasticity
Inositol
Dendrites
Green Fluorescent Proteins
Actin Cytoskeleton
Endoplasmic Reticulum
Glutamic Acid
Microscopy

Keywords

  • CA1
  • Cytochalasin
  • Hippocampus
  • Inositol
  • Rat

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Calcium-triggered exit of F-actin and IP3 3-kinase A from dendritic spines is rapid and reversible. / Schell, Michael J.; Irvine, Robin F.

In: European Journal of Neuroscience, Vol. 24, No. 9, 11.2006, p. 2491-2503.

Research output: Contribution to journalArticle

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