Glucocerebrosidase deficiency in substantia nigra of parkinson disease brains

Ann Neurol. 2012 Sep;72(3):455-63. doi: 10.1002/ana.23614.

Abstract

Objective: Mutations in the glucocerebrosidase gene (GBA) represent a significant risk factor for developing Parkinson disease (PD). We investigated the enzymatic activity of glucocerebrosidase (GCase) in PD brains carrying heterozygote GBA mutations (PD+GBA) and sporadic PD brains.

Methods: GCase activity was measured using a fluorescent assay in cerebellum, frontal cortex, putamen, amygdala, and substantia nigra of PD+GBA (n = 9-14) and sporadic PD brains (n = 12-14). Protein expression of GCase and other lysosomal proteins was determined by western blotting. The relation between GCase, α-synuclein, and mitochondria function was also investigated in vitro.

Results: A significant decrease in GCase activity was observed in all PD+GBA brain areas except the frontal cortex. The greatest deficiency was in the substantia nigra (58% decrease; p < 0.01). GCase activity was also significantly decreased in the substantia nigra (33% decrease; p < 0.05) and cerebellum (24% decrease; p < 0.05) of sporadic PD brains. GCase protein expression was lower in PD+GBA and PD brains, whereas increased C/EBP homologous protein and binding immunoglobulin protein levels indicated that the unfolded protein response was activated. Elevated α-synuclein levels or PTEN-induced putative kinase 1 deficiency in cultured cells had a significant effect on GCase protein levels.

Interpretation: GCase deficiency in PD brains with GBA mutations is a combination of decreased catalytic activity and reduced protein levels. This is most pronounced in the substantia nigra. Biochemical changes involved in PD pathogenesis affect wild-type GCase protein expression in vitro, and these could be contributing factors to the GCase deficiency observed in sporadic PD brains.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Cell Line, Tumor
  • Female
  • Gaucher Disease / complications
  • Gaucher Disease / genetics*
  • Gaucher Disease / pathology*
  • Gene Expression Regulation, Enzymologic / genetics
  • Glucosylceramidase / genetics
  • Glucosylceramidase / metabolism*
  • Heterozygote
  • Humans
  • Immunoprecipitation
  • Male
  • Middle Aged
  • Mitochondria / enzymology
  • Mutation*
  • Neuroblastoma
  • Parkinson Disease / complications
  • Parkinson Disease / pathology*
  • Protein Kinases / deficiency
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Substantia Nigra / enzymology
  • Substantia Nigra / pathology*
  • alpha-Synuclein / metabolism

Substances

  • RNA, Small Interfering
  • alpha-Synuclein
  • Protein Kinases
  • PTEN-induced putative kinase
  • Glucosylceramidase