Novel HCN2 mutation contributes to febrile seizures by shifting the channel's kinetics in a temperature-dependent manner

PLoS One. 2013 Dec 4;8(12):e80376. doi: 10.1371/journal.pone.0080376. eCollection 2013.

Abstract

Hyperpolarization-activated cyclic nucleotide-gated (HCN) channel-mediated currents, known as I h, are involved in the control of rhythmic activity in neuronal circuits and in determining neuronal properties including the resting membrane potential. Recent studies have shown that HCN channels play a role in seizure susceptibility and in absence and limbic epilepsy including temporal lobe epilepsy following long febrile seizures (FS). This study focused on the potential contributions of abnormalities in the HCN2 isoform and their role in FS. A novel heterozygous missense mutation in HCN2 exon 1 leading to p.S126L was identified in two unrelated patients with FS. The mutation was inherited from the mother who had suffered from FS in a pedigree. To determine the effect of this substitution we conducted whole-cell patch clamp electrophysiology. We found that mutant channels had elevated sensitivity to temperature. More specifically, they displayed faster kinetics at higher temperature. Kinetic shift by change of temperature sensitivity rather than the shift of voltage dependence led to increased availability of I h in conditions promoting FS. Responses to cyclic AMP did not differ between wildtype and mutant channels. Thus, mutant HCN2 channels cause significant cAMP-independent enhanced availability of I h during high temperatures, which may contribute to hyperthermia-induced neuronal hyperexcitability in some individuals with FS.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Case-Control Studies
  • Child
  • Cyclic AMP / metabolism
  • Exons*
  • HEK293 Cells
  • Humans
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / genetics*
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / metabolism
  • Kinetics
  • Membrane Potentials
  • Mice
  • Molecular Sequence Data
  • Mutation*
  • Patch-Clamp Techniques
  • Pedigree
  • Potassium Channels / genetics*
  • Potassium Channels / metabolism
  • Rats
  • Seizures, Febrile / genetics*
  • Seizures, Febrile / metabolism
  • Seizures, Febrile / pathology
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Temperature

Substances

  • HCN2 protein, human
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Potassium Channels
  • Cyclic AMP