Dysregulated autophagy contributes to podocyte damage in Fabry's disease

PLoS One. 2013 May 17;8(5):e63506. doi: 10.1371/journal.pone.0063506. Print 2013.

Abstract

Fabry's disease results from an inborn error of glycosphingolipid metabolism that is due to deficiency of the lysosomal hydrolase α-galactosidase A. This X-linked defect results in the accumulation of enzyme substrates with terminally α-glycosidically bound galactose, mainly the neutral glycosphingolipid Globotriaosylceramide (Gb3) in various tissues, including the kidneys. Although end-stage renal disease is one of the most common causes of death in hemizygous males with Fabry's disease, the pathophysiology leading to proteinuria, hematuria, hypertension, and kidney failure is not well understood. Histological studies suggest that the accumulation of Gb3 in podocytes plays an important role in the pathogenesis of glomerular damage. However, due to the lack of appropriate animal or cellular models, podocyte damage in Fabry's disease could not be directly studied yet. As murine models are insufficient, a human model is needed. Here, we developed a human podocyte model of Fabry's disease by combining RNA interference technology with lentiviral transduction of human podocytes. Knockdown of α-galactosidase A expression resulted in diminished enzymatic activity and slowly progressive accumulation of intracellular Gb3. Interestingly, these changes were accompanied by an increase in autophagosomes as indicated by an increased abundance of LC3-II and a loss of mTOR kinase activity, a negative regulator of the autophagic machinery. These data suggest that dysregulated autophagy in α-galactosidase A-deficient podocytes may be the result of deficient mTOR kinase activity. This finding links the lysosomal enzymatic defect in Fabry's disease to deregulated autophagy pathways and provides a promising new direction for further studies on the pathomechanism of glomerular injury in Fabry patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autophagy / physiology*
  • DNA Primers / genetics
  • Fabry Disease / physiopathology*
  • Fluorescent Antibody Technique
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Humans
  • In Situ Nick-End Labeling
  • Luciferases
  • Macrolides
  • Male
  • Models, Biological*
  • Podocytes / metabolism
  • Podocytes / pathology*
  • RNA Interference
  • Real-Time Polymerase Chain Reaction
  • Sirolimus
  • TOR Serine-Threonine Kinases / metabolism
  • Trihexosylceramides / metabolism*
  • alpha-Galactosidase / genetics

Substances

  • DNA Primers
  • Macrolides
  • Trihexosylceramides
  • bafilomycin A
  • globotriaosylceramide
  • Luciferases
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • alpha-Galactosidase
  • Sirolimus

Grants and funding

This study was supported by the Deutsche Forschungsgemeinschaft (grants DFG SFB 635, DFG SFB 829 to T.B.), by Köln Fortune (grant to F.B. and K.H.), by Deutsche Nierenstiftung (grant to K.H.) and by Shire (Grant to T.B. and M.C.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.