Rats harboring S284L Chrna4 mutation show attenuation of synaptic and extrasynaptic GABAergic transmission and exhibit the nocturnal frontal lobe epilepsy phenotype

J Neurosci. 2008 Nov 19;28(47):12465-76. doi: 10.1523/JNEUROSCI.2961-08.2008.

Abstract

Mutations of genes encoding alpha4, beta2, or alpha2 subunits (CHRNA4, CHRNB2, or CHRNA2, respectively) of nAChR [neuronal nicotinic ACh (acetylcholine) receptor] cause nocturnal frontal lobe epilepsy (NFLE) in human. NFLE-related seizures are seen exclusively during sleep and are characterized by three distinct seizure phenotypes: "paroxysmal arousals," "paroxysmal dystonia," and "episodic wandering." We generated transgenic rat strains that harbor a missense mutation S284L, which had been identified in CHRNA4 in NFLE. The transgenic rats were free of biological abnormalities, such as dysmorphology in the CNS, and behavioral abnormalities. The mRNA level of the transgene (mutant Chrna4) was similar to the wild type, and no distorted expression was detected in the brain. However, the transgenic rats showed epileptic seizure phenotypes during slow-wave sleep (SWS) similar to those in NFLE exhibiting three characteristic seizure phenotypes and thus fulfilled the diagnostic criteria of human NFLE. The therapeutic response of these rats to conventional antiepileptic drugs also resembled that of NFLE patients with the S284L mutation. The rats exhibited two major abnormalities in neurotransmission: (1) attenuation of synaptic and extrasynaptic GABAergic transmission and (2) abnormal glutamate release during SWS. The currently available genetically engineered animal models of epilepsy are limited to mice; thus, our transgenic rats offer another dimension to the epilepsy research field.

MeSH terms

  • Age Factors
  • Analysis of Variance
  • Animals
  • Behavior, Animal / physiology
  • Cerebral Cortex / cytology
  • Cerebral Cortex / pathology
  • Dose-Response Relationship, Drug
  • Electroencephalography
  • Epilepsy, Frontal Lobe / diet therapy
  • Epilepsy, Frontal Lobe / genetics*
  • Epilepsy, Frontal Lobe / physiopathology
  • Excitatory Amino Acid Antagonists / pharmacology
  • GABA Antagonists / pharmacology
  • Glutamic Acid / metabolism
  • Hot Temperature / adverse effects
  • In Vitro Techniques
  • Leucine / genetics*
  • Microscopy, Immunoelectron
  • Motor Activity / genetics
  • Motor Skills / physiology
  • Mutation / genetics*
  • Neurotransmitter Agents / metabolism
  • Nicotine / pharmacology
  • Pain Measurement / methods
  • Pentylenetetrazole / pharmacology
  • Phenotype
  • Rats
  • Rats, Transgenic
  • Receptors, Nicotinic / genetics*
  • Receptors, Nicotinic / metabolism
  • Receptors, Nicotinic / ultrastructure
  • Serine / genetics*
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / genetics*
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Neurotransmitter Agents
  • Receptors, Nicotinic
  • nicotinic acetylcholine receptor alpha4 subunit
  • Glutamic Acid
  • Serine
  • gamma-Aminobutyric Acid
  • Nicotine
  • Leucine
  • Pentylenetetrazole