Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction

J Neurosci. 2004 Nov 24;24(47):10750-62. doi: 10.1523/JNEUROSCI.3300-04.2004.

Abstract

Hyperpolarization-activated cation currents (I(h)) are carried by channels encoded by a family of four genes (HCN1-4) that are differentially expressed within the brain in specific cellular and subcellular compartments. HCN1 shows a high level of expression in apical dendrites of cortical pyramidal neurons and in presynaptic terminals of cerebellar basket cells, structures with a high density of I(h). Expression of I(h) is also regulated by neuronal activity. To isolate proteins that may control HCN channel expression or function, we performed yeast two-hybrid screens using the C-terminal cytoplasmic tails of the HCN proteins as bait. We identified a brain-specific protein, which has been previously termed TRIP8b (for TPR-containing Rab8b interacting protein) and PEX5Rp (for Pex5p-related protein), that specifically interacts with all four HCN channels through a conserved sequence in their C-terminal tails. In situ hybridization and immunohistochemistry show that TRIP8b and HCN1 are colocalized, particularly within dendritic arbors of hippocampal CA1 and neocortical layer V pyramidal neurons. The dendritic expression of TRIP8b in layer V pyramidal neurons is disrupted after deletion of HCN1 through homologous recombination, demonstrating a key in vivo interaction between HCN1 and TRIP8b. TRIP8b dramatically alters the trafficking of HCN channels heterologously expressed in Xenopus oocytes and human embryonic kidney 293 cells, causing a specific decrease in surface expression of HCN protein and I(h) density, with a pronounced intracellular accumulation of HCN protein that is colocalized in discrete cytoplasmic clusters with TRIP8b. Finally, TRIP8b expression in cultured pyramidal neurons markedly decreases native I(h) density. These data suggest a possible role for TRIP8b in regulating HCN channel density in the plasma membrane.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Action Potentials / physiology
  • Amino Acid Motifs
  • Amino Acid Sequence
  • Animals
  • Brain / metabolism
  • Cells, Cultured
  • Conserved Sequence
  • Cricetinae
  • Gene Expression Regulation / physiology
  • Humans
  • Ion Channels / biosynthesis*
  • Ion Channels / chemistry
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Knockout
  • Molecular Sequence Data
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / metabolism
  • Nerve Tissue Proteins / physiology*
  • Peroxins
  • Protein Binding / physiology
  • Protein Isoforms
  • Protein Transport / physiology
  • Pyramidal Cells / metabolism
  • Pyramidal Cells / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Recombinant Fusion Proteins / biosynthesis
  • Sindbis Virus
  • Xenopus laevis

Substances

  • Ion Channels
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Peroxins
  • Pex5l protein, mouse
  • Protein Isoforms
  • Recombinant Fusion Proteins