Caldendrin Directly Couples Postsynaptic Calcium Signals to Actin Remodeling in Dendritic Spines

Neuron. 2018 Mar 7;97(5):1110-1125.e14. doi: 10.1016/j.neuron.2018.01.046. Epub 2018 Feb 22.

Abstract

Compartmentalization of calcium-dependent plasticity allows for rapid actin remodeling in dendritic spines. However, molecular mechanisms for the spatio-temporal regulation of filamentous actin (F-actin) dynamics by spinous Ca2+-transients are still poorly defined. We show that the postsynaptic Ca2+ sensor caldendrin orchestrates nano-domain actin dynamics that are essential for actin remodeling in the early phase of long-term potentiation (LTP). Steep elevation in spinous [Ca2+]i disrupts an intramolecular interaction of caldendrin and allows cortactin binding. The fast on and slow off rate of this interaction keeps cortactin in an active conformation, and protects F-actin at the spine base against cofilin-induced severing. Caldendrin gene knockout results in higher synaptic actin turnover, altered nanoscale organization of spinous F-actin, defects in structural spine plasticity, LTP, and hippocampus-dependent learning. Collectively, the data indicate that caldendrin-cortactin directly couple [Ca2+]i to preserve a minimal F-actin pool that is required for actin remodeling in the early phase of LTP.

Keywords: F-actin; STED; calcium; caldendrin; cofilin; cortactin; dendritic spines; synaptic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COS Cells
  • Calcium Signaling / physiology*
  • Calcium-Binding Proteins / deficiency*
  • Calcium-Binding Proteins / genetics
  • Cells, Cultured
  • Chlorocebus aethiops
  • Dendritic Spines / chemistry
  • Dendritic Spines / genetics
  • Dendritic Spines / metabolism*
  • HEK293 Cells
  • Hippocampus / chemistry
  • Hippocampus / metabolism
  • Humans
  • Long-Term Potentiation / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Organ Culture Techniques
  • Rats
  • Rats, Wistar
  • Synaptic Potentials / physiology*

Substances

  • Calcium-Binding Proteins
  • Ca2+-binding protein-1