Long-QT syndrome-associated caveolin-3 mutations differentially regulate the hyperpolarization-activated cyclic nucleotide gated channel 4

Physiol Int. 2017 Jun 1;104(2):130-138. doi: 10.1556/2060.104.2017.2.6. Epub 2017 Jun 26.

Abstract

Background Caveolin-3 (cav-3) mutations are linked to the long-QT syndrome (LQTS) causing distinct clinical symptoms. Hyperpolarization-activated cyclic nucleotide channel 4 (HCN4) underlies the pacemaker current If. It associates with cav-3 and both form a macromolecular complex. Methods To examine the effects of human LQTS-associated cav-3 mutations on HCN4-channel function, HEK293-cells were cotransfected with HCN4 and wild-type (WT) cav-3 or a LQTS-associated cav-3 mutant (T78M, A85T, S141R, or F97C). HCN4 currents were recorded using the whole-cell patch-clamp technique. Results WT cav-3 significantly decreased HCN4 current density and shifted midpoint of activation into negative direction. HCN4 current properties were differentially modulated by LQTS-associated cav-3 mutations. When compared with WT cav-3, A85T, F97C, and T78M did not alter the specific effect of cav-3, but S141R significantly increased HCN4 current density. Compared with WT cav-3, no significant modifications of voltage dependence of steady-state activation curves were observed. However, while WT cav-3 alone had no significant effect on HCN4 current activation, all LQTS-associated cav-3 mutations significantly accelerated HCN4 activation kinetics. Conclusions Our results indicate that HCN4 channel function is modulated by cav-3. LQTS-associated mutations of cav-3 differentially influence pacemaker current properties indicating a pathophysiological role in clinical manifestations.

Keywords: If; caveolin-3; hyperpolarization-activated cyclic nucleotide gated channel 4; long-QT syndrome; whole-cell current.

MeSH terms

  • Action Potentials*
  • Caveolin 3 / genetics
  • Caveolin 3 / metabolism*
  • Gene Expression Regulation / physiology
  • Genetic Predisposition to Disease / genetics
  • HEK293 Cells
  • Humans
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / metabolism*
  • Ion Channel Gating
  • Long QT Syndrome / genetics*
  • Long QT Syndrome / physiopathology*
  • Membrane Potentials
  • Muscle Proteins / metabolism*
  • Mutagenesis, Site-Directed
  • Potassium / metabolism
  • Potassium Channels / metabolism*
  • Structure-Activity Relationship

Substances

  • CAV3 protein, human
  • Caveolin 3
  • HCN4 protein, human
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Muscle Proteins
  • Potassium Channels
  • Potassium