Dynamin- and Rab5-dependent endocytosis of a Ca2+ -activated K+ channel, KCa2.3

PLoS One. 2012;7(8):e44150. doi: 10.1371/journal.pone.0044150. Epub 2012 Aug 28.

Abstract

Regulation of the number of ion channels at the plasma membrane is a critical component of the physiological response. We recently demonstrated that the Ca(2+)-activated K(+) channel, KCa2.3 is rapidly endocytosed and enters a Rab35- and EPI64C-dependent recycling compartment. Herein, we addressed the early endocytic steps of KCa2.3 using a combination of fluorescence and biotinylation techniques. We demonstrate that KCa2.3 is localized to caveolin-rich domains of the plasma membrane using fluorescence co-localization, transmission electron microscopy and co-immunoprecipitation (co-IP). Further, in cells lacking caveolin-1, we observed an accumulation of KCa2.3 at the plasma membrane as well as a decreased rate of endocytosis, as assessed by biotinylation. We also demonstrate that KCa2.3 and dynamin II are co-localized following endocytosis as well as demonstrating they are associated by co-IP. Further, expression of K44A dynamin II resulted in a 2-fold increase in plasma membrane KCa2.3 as well as a 3-fold inhibition of endocytosis. Finally, we evaluated the role of Rab5 in the endocytosis of KCa2.3. We demonstrate that expression of a dominant active Rab5 (Q79L) results in the accumulation of newly endocytosed KCa2.3 on to the membrane of the Rab5-induced vacuoles. We confirmed this co-localization by co-IP; demonstrating that KCa2.3 and Rab5 are associated. As expected, if Rab5 is required for the endocytosis of KCa2.3, expression of a dominant negative Rab5 (S34N) resulted in an approximate 2-fold accumulation of KCa2.3 at the plasma membrane. This was confirmed by siRNA-mediated knockdown of Rab5. Expression of the dominant negative Rab5 also resulted in a decreased rate of KCa2.3 endocytosis. These results demonstrate that KCa2.3 is localized to a caveolin-rich domain within the plasma membrane and is endocytosed in a dynamin- and Rab5-dependent manner prior to entering the Rab35/EPI64C recycling compartment and returning to the plasma membrane.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Caveolae / drug effects
  • Caveolae / metabolism
  • Caveolae / ultrastructure
  • Dynamins / metabolism*
  • Endocytosis*
  • Endosomes / metabolism
  • Endosomes / ultrastructure
  • HEK293 Cells
  • Humans
  • Membrane Microdomains / drug effects
  • Membrane Microdomains / metabolism
  • Mice
  • Models, Biological
  • Potassium Channels, Calcium-Activated / metabolism*
  • Potassium Channels, Calcium-Activated / ultrastructure
  • Protein Transport
  • rab5 GTP-Binding Proteins / metabolism*

Substances

  • Potassium Channels, Calcium-Activated
  • rab5 GTP-Binding Proteins
  • Dynamins