Tubulin binds to the cytoplasmic loop of TRESK background K⁺ channel in vitro

PLoS One. 2014 May 15;9(5):e97854. doi: 10.1371/journal.pone.0097854. eCollection 2014.

Abstract

The cytoplasmic loop between the second and third transmembrane segments is pivotal in the regulation of TRESK (TWIK-related spinal cord K+ channel, K2P18.1, KCNK18). Calcineurin binds to this region and activates the channel by dephosphorylation in response to the calcium signal. Phosphorylation-dependent anchorage of 14-3-3 adaptor protein also modulates TRESK at this location. In the present study, we identified molecular interacting partners of the intracellular loop. By an affinity chromatography approach using the cytoplasmic loop as bait, we have verified the specific association of calcineurin and 14-3-3 to the channel. In addition to these known interacting proteins, we observed substantial binding of tubulin to the intracellular loop. Successive truncation of the polypeptide and pull-down experiments from mouse brain cytosol narrowed down the region sufficient for the binding of tubulin to a 16 amino acid sequence: LVLGRLSYSIISNLDE. The first six residues of this sequence are similar to the previously reported tubulin-binding region of P2X2 purinergic receptor. The tubulin-binding site of TRESK is located close to the protein kinase A (PKA)-dependent 14-3-3-docking motif of the channel. We provide experimental evidence suggesting that 14-3-3 competes with tubulin for the binding to the cytoplasmic loop of TRESK. It is intriguing that the 16 amino acid tubulin-binding sequence includes the serines, which were previously shown to be phosphorylated by microtubule-affinity regulating kinases (MARK kinases) and contribute to channel inhibition. Although tubulin binds to TRESK in vitro, it remains to be established whether the two proteins also interact in the living cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / chemistry
  • Amino Acid Sequence
  • Animals
  • Avian Proteins / chemistry
  • Binding, Competitive
  • Calcineurin / chemistry
  • Chickens
  • Chromatography, Affinity
  • Humans
  • Mice
  • Molecular Sequence Data
  • Peptide Fragments / chemistry
  • Potassium Channels / chemistry*
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Tubulin / chemistry*
  • Zebrafish
  • Zebrafish Proteins / chemistry

Substances

  • 14-3-3 Proteins
  • Avian Proteins
  • Peptide Fragments
  • Potassium Channels
  • Trik protein, mouse
  • Tubulin
  • Zebrafish Proteins
  • Calcineurin

Grants and funding

This work was supported by the Hungarian National Research Fund OTKA K108496. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.