Neuronal hyperexcitability in a mouse model of SCN8A epileptic encephalopathy

Proc Natl Acad Sci U S A. 2017 Feb 28;114(9):2383-2388. doi: 10.1073/pnas.1616821114. Epub 2017 Feb 13.

Abstract

Patients with early infantile epileptic encephalopathy (EIEE) experience severe seizures and cognitive impairment and are at increased risk for sudden unexpected death in epilepsy (SUDEP). EIEE13 [Online Mendelian Inheritance in Man (OMIM) # 614558] is caused by de novo missense mutations in the voltage-gated sodium channel gene SCN8A Here, we investigated the neuronal phenotype of a mouse model expressing the gain-of-function SCN8A patient mutation, p.Asn1768Asp (Nav1.6-N1768D). Our results revealed regional and neuronal subtype specificity in the effects of the N1768D mutation. Acutely dissociated hippocampal neurons from Scn8aN1768D/+ mice showed increases in persistent sodium current (INa) density in CA1 pyramidal but not bipolar neurons. In CA3, INa,P was increased in both bipolar and pyramidal neurons. Measurement of action potential (AP) firing in Scn8aN1768D/+ pyramidal neurons in brain slices revealed early afterdepolarization (EAD)-like AP waveforms in CA1 but not in CA3 hippocampal or layer II/III neocortical neurons. The maximum spike frequency evoked by depolarizing current injections in Scn8aN1768D/+ CA1, but not CA3 or neocortical, pyramidal cells was significantly reduced compared with WT. Spontaneous firing was observed in subsets of neurons in CA1 and CA3, but not in the neocortex. The EAD-like waveforms of Scn8aN1768D/+ CA1 hippocampal neurons were blocked by tetrodotoxin, riluzole, and SN-6, implicating elevated persistent INa and reverse mode Na/Ca exchange in the mechanism of hyperexcitability. Our results demonstrate that Scn8a plays a vital role in neuronal excitability and provide insight into the mechanism and future treatment of epileptogenesis in EIEE13.

Keywords: Na/Ca exchange; action potential; epilepsy; mouse model; sodium channel.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / drug effects
  • Amino Acid Substitution
  • Animals
  • Benzyl Compounds / pharmacology
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / metabolism*
  • CA1 Region, Hippocampal / pathology
  • CA3 Region, Hippocampal / drug effects
  • CA3 Region, Hippocampal / metabolism
  • CA3 Region, Hippocampal / pathology
  • Disease Models, Animal
  • Gene Expression
  • Humans
  • Mice
  • Mice, Transgenic
  • Mutation*
  • NAV1.6 Voltage-Gated Sodium Channel / genetics*
  • NAV1.6 Voltage-Gated Sodium Channel / metabolism
  • Neocortex / drug effects
  • Neocortex / metabolism
  • Neocortex / pathology
  • Organ Specificity
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism*
  • Pyramidal Cells / pathology
  • Riluzole / pharmacology
  • Sodium Channel Blockers / pharmacology
  • Spasms, Infantile / genetics*
  • Spasms, Infantile / metabolism
  • Spasms, Infantile / physiopathology
  • Tetrodotoxin / pharmacology
  • Thiazolidines / pharmacology

Substances

  • 2-(4-(4-nitrobenzyloxy)benzyl)thiazolidine-4-carboxylic acid ethyl ester
  • Benzyl Compounds
  • NAV1.6 Voltage-Gated Sodium Channel
  • Scn8a protein, mouse
  • Sodium Channel Blockers
  • Thiazolidines
  • Tetrodotoxin
  • Riluzole

Supplementary concepts

  • Infantile Epileptic-Dyskinetic Encephalopathy