Mutant SNAP25B causes myasthenia, cortical hyperexcitability, ataxia, and intellectual disability

Neurology. 2014 Dec 9;83(24):2247-55. doi: 10.1212/WNL.0000000000001079. Epub 2014 Nov 7.

Abstract

Objective: To identify and characterize the molecular basis of a syndrome associated with myasthenia, cortical hyperexcitability, cerebellar ataxia, and intellectual disability.

Methods: We performed in vitro microelectrode studies of neuromuscular transmission, performed exome and Sanger sequencing, and analyzed functional consequences of the identified mutation in expression studies.

Results: Neuromuscular transmission at patient endplates was compromised by reduced evoked quantal release. Exome sequencing identified a dominant de novo variant, p.Ile67Asn, in SNAP25B, a SNARE protein essential for exocytosis of synaptic vesicles from nerve terminals and of dense-core vesicles from endocrine cells. Ca(2+)-triggered exocytosis is initiated when synaptobrevin attached to synaptic vesicles (v-SNARE) assembles with SNAP25B and syntaxin anchored in the presynaptic membrane (t-SNAREs) into an α-helical coiled-coil held together by hydrophobic interactions. Pathogenicity of the Ile67Asn mutation was confirmed by 2 measures. First, the Ca(2+) triggered fusion of liposomes incorporating v-SNARE with liposomes containing t-SNAREs was hindered when t-SNAREs harbored the mutant SNAP25B moiety. Second, depolarization of bovine chromaffin cells transfected with mutant SNAP25B or with mutant plus wild-type SNAP25B markedly reduced depolarization-evoked exocytosis compared with wild-type transfected cells.

Conclusion: Ile67Asn variant in SNAP25B is pathogenic because it inhibits synaptic vesicle exocytosis. We attribute the deleterious effects of the mutation to disruption of the hydrophobic α-helical coiled-coil structure of the SNARE complex by replacement of a highly hydrophobic isoleucine by a strongly hydrophilic asparagine.

Publication types

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

MeSH terms

  • Adolescent
  • Animals
  • Ataxia / genetics*
  • Ataxia / physiopathology
  • Brain Diseases / genetics*
  • Brain Diseases / physiopathology
  • COS Cells
  • Cattle
  • Chlorocebus aethiops
  • Chromaffin Cells / physiology
  • DNA Mutational Analysis
  • Exocytosis / physiology
  • Female
  • Humans
  • Intellectual Disability / genetics*
  • Intellectual Disability / physiopathology
  • Microelectrodes
  • Motor Endplate / physiopathology
  • Mutation
  • SNARE Proteins / metabolism
  • Synaptic Vesicles / physiology
  • Synaptosomal-Associated Protein 25 / genetics*
  • Synaptosomal-Associated Protein 25 / metabolism
  • Syndrome
  • Transfection

Substances

  • SNAP25 protein, human
  • SNARE Proteins
  • Synaptosomal-Associated Protein 25