Coupled activity-dependent trafficking of synaptic SK2 channels and AMPA receptors

Mike T. Lin, Rafael Luján, Masahiko Watanabe, Matthew Frerking, James Maylie, John Adelman

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Small conductance Ca2+-activated K+ type 2 (SK2) channels are expressed in the postsynaptic density of CA1 neurons where they are activated by synaptically evoked Ca2+ influx to limit the size of EPSPs and spine Ca2+ transients. At Schaffer collateral synapses, the induction of long-term potentiation (LTP) increases the α-amino-3- hydroxyl-5-methyl-4-isoxazole-propionate receptor (AMPAR)-mediated contribution to synaptic transmission and decreases the synaptic SK2 channel contribution through protein kinase A-dependent channel endocytosis. Using a combination of electrophysiology and immunoelectron microscopy in mice, the relationship between the dynamics of spine SK2 channels and AMPARs was investigated. Unlike AMPARs, synaptic SK2 channels under basal conditions do not rapidly recycle. Furthermore, SK2 channels occupy a distinct population of endosomes separate from AMPARs. However, blocking vesicular exocytosis or the delivery of synaptic GluA1-containing AMPARs during the induction of LTP blocks SK2 channel endocytosis. By ∼2 h after the induction of LTP, synaptic SK2 channel expression and function are restored. Thus, LTP-dependent endocytosis of SK2 is coupled to LTP-dependent AMPA exocytosis, and the ∼2 h window after the induction of LTP during which synaptic SK2 activity is absent may be important for consolidating the later phases of LTP.

Original languageEnglish (US)
Pages (from-to)11726-11734
Number of pages9
JournalJournal of Neuroscience
Volume30
Issue number35
DOIs
StatePublished - Sep 1 2010

Fingerprint

AMPA Receptors
Long-Term Potentiation
Endocytosis
Exocytosis
Spine
Isoxazoles
Post-Synaptic Density
Immunoelectron Microscopy
Excitatory Postsynaptic Potentials
Electrophysiology
Endosomes
Propionates
Cyclic AMP-Dependent Protein Kinases
Synaptic Transmission
Hydroxyl Radical
Synapses
Hippocampus
Neurons
Population

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)

Cite this

Coupled activity-dependent trafficking of synaptic SK2 channels and AMPA receptors. / Lin, Mike T.; Luján, Rafael; Watanabe, Masahiko; Frerking, Matthew; Maylie, James; Adelman, John.

In: Journal of Neuroscience, Vol. 30, No. 35, 01.09.2010, p. 11726-11734.

Research output: Contribution to journalArticle

Lin, Mike T. ; Luján, Rafael ; Watanabe, Masahiko ; Frerking, Matthew ; Maylie, James ; Adelman, John. / Coupled activity-dependent trafficking of synaptic SK2 channels and AMPA receptors. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 35. pp. 11726-11734.
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