In Vitro Analyses of Novel HCN4 Gene Mutations

Cell Physiol Biochem. 2018;49(3):1197-1207. doi: 10.1159/000493301. Epub 2018 Sep 7.

Abstract

Background/aims: The hyperpolarization-activated cyclic nucleotide-gated cation channel HCN4 contributes significantly to the generation of basic cardiac electrical activity in the sinus node and is a mediator of modulation by β-adrenergic stimulation. Heterologous expression of sick sinus syndrome (SSS) and bradycardia associated mutations within the human HCN4 gene results in altered channel function. The main aim was to describe the functional characterization of three (two novel and one known) missense mutations of HCN4 identified in families with SSS.

Methods: Here, the two-electrode voltage clamp technique on Xenopus laevis oocytes and confocal imaging on transfected COS7 cells respectively, were used to analyze the functional effects of three HCN4 mutations; R378C, R550H, and E1193Q. Membrane surface expressions of wild type and the mutant channels were assessed by confocal microscopy, chemiluminescence assay, and Western blot in COS7 and HeLa cells.

Results: The homomeric mutant channels R550H and E1193Q showed loss of function through increased rates of deactivation and distinctly reduced surface expression in all three homomeric mutant channels. HCN4 channels containing R550H and E1193Q mutant subunits only showed minor effects on the voltage dependence and rates of activation/deactivation. In contrast, homomeric R378C exerted a left-shifted activation curve and slowed activation kinetics. These effects were reduced in heteromeric co-expression of R378C with wild-type (WT) channels.

Conclusion: Dysfunction of homomeric/heteromeric mutant HCN4-R378C, R550H, and E1193Q channels in the present study was primarily caused by loss of function due to decreased channel surface expression.

Keywords: Arrhythmias; Bradycardia; Channelopathy; Disease; Funny current (If); HCN Channels; Heart; Pacemaking; Rhythm.

MeSH terms

  • Action Potentials / physiology
  • Animals
  • COS Cells
  • Chlorocebus aethiops
  • HeLa Cells
  • Humans
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / chemistry
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / genetics
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / metabolism*
  • Microscopy, Confocal
  • Molecular Dynamics Simulation
  • Muscle Proteins / chemistry
  • Muscle Proteins / genetics*
  • Muscle Proteins / metabolism*
  • Mutagenesis, Site-Directed
  • Oocytes / metabolism
  • Patch-Clamp Techniques
  • Potassium Channels / chemistry
  • Potassium Channels / genetics*
  • Potassium Channels / metabolism*
  • Protein Structure, Tertiary
  • Sick Sinus Syndrome / genetics*
  • Xenopus laevis

Substances

  • HCN4 protein, human
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Muscle Proteins
  • Potassium Channels