Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons

D. E. Antonucci, S. T. Lim, S. Vassanelli, James Trimmer

Research output: Contribution to journalArticle

80 Citations (Scopus)

Abstract

Dendritic excitability is modulated by the highly variable spatial and temporal expression pattern of voltage-dependent potassium channels. Somatodendritic Kv2.1 channels contribute a major component of delayed rectifier potassium current in cultured hippocampal neurons, where Kv2.1 is localized to large clusters on the soma and proximal dendrites. Here we found that dramatic differences exist in the clustering of endogenous Kv2.1 in cultured rat hippocampal GABAergic interneurons and glutamatergic pyramidal neurons. Studies on neurons developing in culture revealed that while a similar sequence of Kv2.1 localization and clustering occurred in both cell types, the process was temporally delayed in pyramidal cells. Localization and clustering of recombinant green fluorescent protein-tagged Kv2.1 occurred by the same sequence of events, and imaging of GFP-Kv2.1 clustering in living neurons revealed dynamic fusion events that underlie cluster formation. Overexpression of GFP-Kv2.1 accelerated the clustering program in pyramidal neurons such that the observed differences in Kv2.1 clustering in pyramidal neurons and interneurons were eliminated. Confocal imaging showed a preferential association of Kv2.1 with the basal membrane in cultured neurons, and electrophysiological recordings from neurons cultured on transistors revealed that Kv2.1 contributed the bulk of a previously described adherens junction delayed rectifier potassium conductance. Finally, Kv2.1 clusters were found spatially associated with ryanodine receptor intracellular Ca2+ ([Ca2+]i) release channels. These findings reveal a stepwise assembly of Kv2.1 potassium channels into membrane clusters during development, and an association of these clusters with Ca2+ signaling apparatus. Together these data suggest that the restricted localization of Kv2.1 may play an important role in the previously observed contribution of this potassium channel in regulating dendritic [Ca2+]i transients.

Original languageEnglish (US)
Pages (from-to)69-81
Number of pages13
JournalNeuroscience
Volume108
Issue number1
DOIs
StatePublished - Dec 5 2001
Externally publishedYes

Fingerprint

Potassium Channels
Cluster Analysis
Pyramidal Cells
Neurons
Interneurons
Shab Potassium Channels
Potassium
Adherens Junctions
Ryanodine Receptor Calcium Release Channel
Membranes
Carisoprodol
Dendrites
Green Fluorescent Proteins
Recombinant Proteins

Keywords

  • Dendritic excitability
  • Immunohistochemistry
  • Interneuron
  • Patch-clamp
  • Pyramidal cell

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. / Antonucci, D. E.; Lim, S. T.; Vassanelli, S.; Trimmer, James.

In: Neuroscience, Vol. 108, No. 1, 05.12.2001, p. 69-81.

Research output: Contribution to journalArticle

Antonucci, D. E. ; Lim, S. T. ; Vassanelli, S. ; Trimmer, James. / Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. In: Neuroscience. 2001 ; Vol. 108, No. 1. pp. 69-81.
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