Viable neuronopathic Gaucher disease model in Medaka (Oryzias latipes) displays axonal accumulation of alpha-synuclein

PLoS Genet. 2015 Apr 2;11(4):e1005065. doi: 10.1371/journal.pgen.1005065. eCollection 2015 Apr.

Abstract

Homozygous mutations in the glucocerebrosidase (GBA) gene result in Gaucher disease (GD), the most common lysosomal storage disease. Recent genetic studies have revealed that GBA mutations confer a strong risk for sporadic Parkinson's disease (PD). To investigate how GBA mutations cause PD, we generated GBA nonsense mutant (GBA-/-) medaka that are completely deficient in glucocerebrosidase (GCase) activity. In contrast to the perinatal death in humans and mice lacking GCase activity, GBA-/- medaka survived for months, enabling analysis of the pathological progression. GBA-/- medaka displayed the pathological phenotypes resembling human neuronopathic GD including infiltration of Gaucher cell-like cells into the brains, progressive neuronal loss, and microgliosis. Detailed pathological findings represented lysosomal abnormalities in neurons and alpha-synuclein (α-syn) accumulation in axonal swellings containing autophagosomes. Unexpectedly, disruption of α-syn did not improve the life span, formation of axonal swellings, neuronal loss, or neuroinflammation in GBA-/- medaka. Taken together, the present study revealed GBA-/- medaka as a novel neuronopathic GD model, the pahological mechanisms of α-syn accumulation caused by GCase deficiency, and the minimal contribution of α-syn to the pathogenesis of neuronopathic GD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / metabolism*
  • Axons / ultrastructure
  • Disease Models, Animal
  • Gaucher Disease / genetics*
  • Gaucher Disease / metabolism
  • Gaucher Disease / pathology
  • Glucosylceramidase / deficiency*
  • Glucosylceramidase / genetics
  • Oryzias / genetics*
  • Oryzias / metabolism
  • Phagosomes / metabolism
  • alpha-Synuclein / metabolism*

Substances

  • alpha-Synuclein
  • Glucosylceramidase

Grants and funding

This work was supported by Grant-in-Aid for Specially Promoted Research and Scientific Research on Innovative Areas “Brain Environment” from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant Number 23111001, http://www.jsps.go.jp/english/index.html). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.