α-Galactosidase aggregation is a determinant of pharmacological chaperone efficacy on Fabry disease mutants

J Biol Chem. 2012 Aug 17;287(34):28386-97. doi: 10.1074/jbc.M112.351056. Epub 2012 Jul 6.

Abstract

Fabry disease is a lysosomal storage disorder caused by loss of α-galactosidase function. More than 500 Fabry disease mutants have been identified, the majority of which are structurally destabilized. A therapeutic strategy under development for lysosomal storage diseases consists of using pharmacological chaperones to stabilize the structure of the mutant protein, thereby promoting lysosomal delivery over retrograde degradation. The substrate analog 1-deoxygalactonojirimycin (DGJ) has been shown to restore activity of mutant α-galactosidase and is currently in clinical trial for treatment of Fabry disease. However, only ∼65% of tested mutants respond to treatment in cultured patient fibroblasts, and the structural underpinnings of DGJ response remain poorly explained. Using computational modeling and cell culture experiments, we show that the DGJ response is negatively affected by protein aggregation of α-galactosidase mutants, revealing a qualitative difference between misfolding-associated and aggregation-associated loss of function. A scoring function combining predicted thermodynamic stability and intrinsic aggregation propensity of mutants captures well their aggregation behavior under overexpression in HeLa cells. Interestingly, the same classifier performs well on DGJ response data of patient-derived cultured lymphoblasts, showing that protein aggregation is an important determinant of chemical chaperone efficiency under endogenous expression levels as well. Our observations reinforce the idea that treatment of aggregation-associated loss of function observed for the more severe α-galactosidase mutants could be enhanced by combining pharmacological chaperone treatment with the suppression of mutant aggregation, e.g. via proteostatic regulator compounds that increase cellular chaperone expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Deoxynojirimycin / analogs & derivatives*
  • 1-Deoxynojirimycin / pharmacology
  • Enzyme Activation / drug effects
  • Fabry Disease / drug therapy
  • Fabry Disease / genetics
  • Fabry Disease / metabolism*
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Gene Expression Regulation / drug effects*
  • Gene Expression Regulation / genetics
  • HeLa Cells
  • Humans
  • Molecular Chaperones / biosynthesis*
  • Molecular Chaperones / genetics
  • Mutation, Missense*
  • alpha-Galactosidase / genetics
  • alpha-Galactosidase / metabolism*

Substances

  • Molecular Chaperones
  • 1-Deoxynojirimycin
  • migalastat
  • alpha-Galactosidase