Non-conducting function of the Kv2.1 channel enables it to recruit vesicles for release in neuroendocrine and nerve cells

J Cell Sci. 2010 Jun 1;123(Pt 11):1940-7. doi: 10.1242/jcs.063719.

Abstract

Regulation of exocytosis by voltage-gated K(+) channels has classically been viewed as inhibition mediated by K(+) fluxes. We recently identified a new role for Kv2.1 in facilitating vesicle release from neuroendocrine cells, which is independent of K(+) flux. Here, we show that Kv2.1-induced facilitation of release is not restricted to neuroendocrine cells, but also occurs in the somatic-vesicle release from dorsal-root-ganglion neurons and is mediated by direct association of Kv2.1 with syntaxin. We further show in adrenal chromaffin cells that facilitation induced by both wild-type and non-conducting mutant Kv2.1 channels in response to long stimulation persists during successive stimulation, and can be attributed to an increased number of exocytotic events and not to changes in single-spike kinetics. Moreover, rigorous analysis of the pools of released vesicles reveals that Kv2.1 enhances the rate of vesicle recruitment during stimulation with high Ca(2+), without affecting the size of the readily releasable vesicle pool. These findings place a voltage-gated K(+) channel among the syntaxin-binding proteins that directly regulate pre-fusion steps in exocytosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Calcium Signaling
  • Cells, Cultured
  • Chromaffin Cells / metabolism*
  • Chromaffin Cells / pathology
  • Electrophysiology
  • Exocytosis*
  • Ganglia, Spinal / pathology*
  • Neurons / metabolism*
  • Neurons / pathology
  • Qa-SNARE Proteins / metabolism
  • Rats
  • Rats, Wistar
  • Secretory Vesicles / metabolism*
  • Shab Potassium Channels / genetics
  • Shab Potassium Channels / metabolism*

Substances

  • Qa-SNARE Proteins
  • Shab Potassium Channels