Heterozygous reelin mutations cause autosomal-dominant lateral temporal epilepsy

Am J Hum Genet. 2015 Jun 4;96(6):992-1000. doi: 10.1016/j.ajhg.2015.04.020.

Abstract

Autosomal-dominant lateral temporal epilepsy (ADLTE) is a genetic epilepsy syndrome clinically characterized by focal seizures with prominent auditory symptoms. ADLTE is genetically heterogeneous, and mutations in LGI1 account for fewer than 50% of affected families. Here, we report the identification of causal mutations in reelin (RELN) in seven ADLTE-affected families without LGI1 mutations. We initially investigated 13 ADLTE-affected families by performing SNP-array linkage analysis and whole-exome sequencing and identified three heterozygous missense mutations co-segregating with the syndrome. Subsequent analysis of 15 small ADLTE-affected families revealed four additional missense mutations. 3D modeling predicted that all mutations have structural effects on protein-domain folding. Overall, RELN mutations occurred in 7/40 (17.5%) ADLTE-affected families. RELN encodes a secreted protein, Reelin, which has important functions in both the developing and adult brain and is also found in the blood serum. We show that ADLTE-related mutations significantly decrease serum levels of Reelin, suggesting an inhibitory effect of mutations on protein secretion. We also show that Reelin and LGI1 co-localize in a subset of rat brain neurons, supporting an involvement of both proteins in a common molecular pathway underlying ADLTE. Homozygous RELN mutations are known to cause lissencephaly with cerebellar hypoplasia. Our findings extend the spectrum of neurological disorders associated with RELN mutations and establish a link between RELN and LGI1, which play key regulatory roles in both the developing and adult brain.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Cell Adhesion Molecules, Neuronal / blood
  • Cell Adhesion Molecules, Neuronal / chemistry
  • Cell Adhesion Molecules, Neuronal / genetics*
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Chromosome Mapping
  • Epilepsy, Frontal Lobe / genetics*
  • Epilepsy, Frontal Lobe / pathology*
  • Exome
  • Extracellular Matrix Proteins / blood
  • Extracellular Matrix Proteins / chemistry
  • Extracellular Matrix Proteins / genetics*
  • Extracellular Matrix Proteins / metabolism
  • Fluorescent Antibody Technique
  • Gene Components
  • Humans
  • Immunoblotting
  • Intercellular Signaling Peptides and Proteins
  • Models, Molecular*
  • Molecular Sequence Data
  • Mutation, Missense / genetics*
  • Nerve Tissue Proteins / blood
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Pedigree
  • Polymorphism, Single Nucleotide / genetics
  • Protein Conformation
  • Protein Folding
  • Proteins / metabolism
  • Rats
  • Reelin Protein
  • Sequence Analysis, DNA
  • Serine Endopeptidases / blood
  • Serine Endopeptidases / chemistry
  • Serine Endopeptidases / genetics*
  • Serine Endopeptidases / metabolism
  • Sleep Wake Disorders / genetics*
  • Sleep Wake Disorders / pathology*

Substances

  • Cell Adhesion Molecules, Neuronal
  • Extracellular Matrix Proteins
  • Intercellular Signaling Peptides and Proteins
  • Lgi1 protein, rat
  • Nerve Tissue Proteins
  • Proteins
  • Reelin Protein
  • Reln protein, rat
  • RELN protein, human
  • Serine Endopeptidases

Supplementary concepts

  • Autosomal Dominant Lateral Temporal Lobe Epilepsy