Interaction with 14-3-3 proteins promotes functional expression of the potassium channels TASK-1 and TASK-3

J Physiol. 2002 Nov 15;545(1):13-26. doi: 10.1113/jphysiol.2002.027052.

Abstract

The two-pore-domain potassium channels TASK-1, TASK-3 and TASK-5 possess a conserved C-terminal motif of five amino acids. Truncation of the C-terminus of TASK-1 strongly reduced the currents measured after heterologous expression in Xenopus oocytes or HEK293 cells and decreased surface membrane expression of GFP-tagged channel proteins. Two-hybrid analysis showed that the C-terminal domain of TASK-1, TASK-3 and TASK-5, but not TASK-4, interacts with isoforms of the adapter protein 14-3-3. A pentapeptide motif at the extreme C-terminus of TASK-1, RRx(S/T)x, was found to be sufficient for weak but significant interaction with 14-3-3, whereas the last 40 amino acids of TASK-1 were required for strong binding. Deletion of a single amino acid at the C-terminal end of TASK-1 or TASK-3 abolished binding of 14-3-3 and strongly reduced the macroscopic currents observed in Xenopus oocytes. TASK-1 mutants that failed to interact with 14-3-3 isoforms (V411*, S410A, S410D) also produced only very weak macroscopic currents. In contrast, the mutant TASK-1 S409A, which interacts with 14-3-3-like wild-type channels, displayed normal macroscopic currents. Co-injection of 14-3-3zeta cRNA increased TASK-1 current in Xenopus oocytes by about 70 %. After co-transfection in HEK293 cells, TASK-1 and 14-3-3zeta (but not TASK-1DeltaC5 and 14-3-3zeta) could be co-immunoprecipitated. Furthermore, TASK-1 and 14-3-3 could be co-immunoprecipitated in synaptic membrane extracts and postsynaptic density membranes. Our findings suggest that interaction of 14-3-3 with TASK-1 or TASK-3 may promote the trafficking of the channels to the surface membrane.

MeSH terms

  • 14-3-3 Proteins
  • Amino Acid Motifs / physiology
  • Amino Acid Sequence / genetics
  • Animals
  • Biological Transport / physiology
  • COS Cells
  • Cell Line / physiology
  • Cell Membrane / metabolism
  • Electric Conductivity
  • Female
  • Gene Deletion
  • Humans
  • Molecular Sequence Data
  • Mutation / physiology
  • Nerve Tissue Proteins / physiology*
  • Oocytes / physiology
  • Peptide Fragments / genetics
  • Potassium Channels / physiology*
  • Potassium Channels, Tandem Pore Domain*
  • Protein Isoforms / physiology
  • Protein Structure, Tertiary / physiology
  • Rats
  • Tyrosine 3-Monooxygenase / physiology*
  • Xenopus

Substances

  • 14-3-3 Proteins
  • KCNK9 protein, human
  • Kcnk9 protein, rat
  • Nerve Tissue Proteins
  • Peptide Fragments
  • Potassium Channels
  • Potassium Channels, Tandem Pore Domain
  • Protein Isoforms
  • potassium channel subfamily K member 3
  • Tyrosine 3-Monooxygenase