Mutations in potassium channel kcnd3 cause spinocerebellar ataxia type 19

Ann Neurol. 2012 Dec;72(6):870-80. doi: 10.1002/ana.23700.

Abstract

Objective: To identify the causative gene for the neurodegenerative disorder spinocerebellar ataxia type 19 (SCA19) located on chromosomal region 1p21-q21.

Methods: Exome sequencing was used to identify the causal mutation in a large SCA19 family. We then screened 230 ataxia families for mutations located in the same gene (KCND3, also known as Kv4.3) using high-resolution melting. SCA19 brain autopsy material was evaluated, and in vitro experiments using ectopic expression of wild-type and mutant Kv4.3 were used to study protein localization, stability, and channel activity by patch-clamping.

Results: We detected a T352P mutation in the third extracellular loop of the voltage-gated potassium channel KCND3 that cosegregated with the disease phenotype in our original family. We identified 2 more novel missense mutations in the channel pore (M373I) and the S6 transmembrane domain (S390N) in 2 other ataxia families. T352P cerebellar autopsy material showed severe Purkinje cell degeneration, with abnormal intracellular accumulation and reduced protein levels of Kv4.3 in their soma. Ectopic expression of all mutant proteins in HeLa cells revealed retention in the endoplasmic reticulum and enhanced protein instability, in contrast to wild-type Kv4.3 that was localized on the plasma membrane. The regulatory β subunit Kv channel interacting protein 2 was able to rescue the membrane localization and the stability of 2 of the 3 mutant Kv4.3 complexes. However, this either did not restore the channel function of the membrane-located mutant Kv4.3 complexes or restored it only partially.

Interpretation: KCND3 mutations cause SCA19 by impaired protein maturation and/or reduced channel function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Brain / pathology
  • Case-Control Studies
  • Chromatin Immunoprecipitation
  • Cycloheximide / pharmacology
  • DNA Mutational Analysis
  • Disease Progression
  • Family Health
  • Female
  • Genetic Association Studies
  • Genetic Predisposition to Disease*
  • Genotype
  • HEK293 Cells / metabolism
  • HeLa Cells / pathology
  • Humans
  • Luminescent Proteins / genetics
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / genetics
  • Mutation, Missense / genetics*
  • Patch-Clamp Techniques
  • Protein Synthesis Inhibitors / pharmacology
  • Shal Potassium Channels / genetics*
  • Silver Staining
  • Spinocerebellar Degenerations / genetics*
  • Spinocerebellar Degenerations / pathology
  • Time Factors
  • Transfection

Substances

  • Luminescent Proteins
  • Protein Synthesis Inhibitors
  • Shal Potassium Channels
  • Cycloheximide

Supplementary concepts

  • Spinocerebellar ataxia 19