Tay-Sachs disease mutations in HEXA target the α chain of hexosaminidase A to endoplasmic reticulum-associated degradation

Mol Biol Cell. 2016 Dec 1;27(24):3813-3827. doi: 10.1091/mbc.E16-01-0012. Epub 2016 Sep 28.

Abstract

Loss of function of the enzyme β-hexosaminidase A (HexA) causes the lysosomal storage disorder Tay-Sachs disease (TSD). It has been proposed that mutations in the α chain of HexA can impair folding, enzyme assembly, and/or trafficking, yet there is surprisingly little known about the mechanisms of these potential routes of pathogenesis. We therefore investigated the biosynthesis and trafficking of TSD-associated HexA α mutants, seeking to identify relevant cellular quality control mechanisms. The α mutants E482K and G269S are defective in enzymatic activity, unprocessed by lysosomal proteases, and exhibit altered folding pathways compared with wild-type α. E482K is more severely misfolded than G269S, as observed by its aggregation and inability to associate with the HexA β chain. Importantly, both mutants are retrotranslocated from the endoplasmic reticulum (ER) to the cytosol and are degraded by the proteasome, indicating that they are cleared via ER-associated degradation (ERAD). Leveraging these discoveries, we observed that manipulating the cellular folding environment or ERAD pathways can alter the kinetics of mutant α degradation. Additionally, growth of patient fibroblasts at a permissive temperature or with chemical chaperones increases cellular Hex activity by improving mutant α folding. Therefore modulation of the ER quality control systems may be a potential therapeutic route for improving some forms of TSD.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum-Associated Degradation / physiology
  • HEK293 Cells
  • Hexosaminidase A / biosynthesis
  • Hexosaminidase A / genetics*
  • Hexosaminidase A / metabolism*
  • Hexosaminidase A / physiology
  • Humans
  • Lysosomes / metabolism
  • Molecular Chaperones / metabolism
  • Mutation
  • Primary Cell Culture
  • Protein Transport / physiology
  • Proteolysis
  • Tay-Sachs Disease / genetics
  • Tay-Sachs Disease / metabolism
  • beta-N-Acetylhexosaminidases / metabolism

Substances

  • Molecular Chaperones
  • Hexosaminidase A
  • beta-N-Acetylhexosaminidases