β-III spectrin underpins ankyrin R function in Purkinje cell dendritic trees: protein complex critical for sodium channel activity is impaired by SCA5-associated mutations

Hum Mol Genet. 2014 Jul 15;23(14):3875-82. doi: 10.1093/hmg/ddu103. Epub 2014 Mar 6.

Abstract

Beta III spectrin is present throughout the elaborate dendritic tree of cerebellar Purkinje cells and is required for normal neuronal morphology and cell survival. Spinocerebellar ataxia type 5 (SCA5) and spectrin associated autosomal recessive cerebellar ataxia type 1 are human neurodegenerative diseases involving progressive gait ataxia and cerebellar atrophy. Both disorders appear to result from loss of β-III spectrin function. Further elucidation of β-III spectrin function is therefore needed to understand disease mechanisms and identify potential therapeutic options. Here, we report that β-III spectrin is essential for the recruitment and maintenance of ankyrin R at the plasma membrane of Purkinje cell dendrites. Two SCA5-associated mutations of β-III spectrin both reduce ankyrin R levels at the cell membrane. Moreover, a wild-type β-III spectrin/ankyrin-R complex increases sodium channel levels and activity in cell culture, whereas mutant β-III spectrin complexes fail to enhance sodium currents. This suggests impaired ability to form stable complexes between the adaptor protein ankyrin R and its interacting partners in the Purkinje cell dendritic tree is a key mechanism by which mutant forms of β-III spectrin cause ataxia, initially by Purkinje cell dysfunction and exacerbated by subsequent cell death.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ankyrins / metabolism*
  • Cell Membrane / metabolism
  • Cells, Cultured
  • HEK293 Cells
  • Humans
  • Mice
  • Mutation
  • Protein Stability
  • Purkinje Cells / metabolism*
  • Purkinje Cells / ultrastructure
  • Rats
  • Rats, Sprague-Dawley
  • Sodium Channels / physiology*
  • Spectrin / genetics*
  • Spectrin / metabolism*
  • Spinocerebellar Ataxias / genetics*

Substances

  • Ankyrins
  • SPTBN2 protein, mouse
  • Sodium Channels
  • Spectrin