Impaired autophagy in the lipid-storage disorder Niemann-Pick type C1 disease

Cell Rep. 2013 Dec 12;5(5):1302-15. doi: 10.1016/j.celrep.2013.10.042. Epub 2013 Nov 27.

Abstract

Autophagy dysfunction has been implicated in misfolded protein accumulation and cellular toxicity in several diseases. Whether alterations in autophagy also contribute to the pathology of lipid-storage disorders is not clear. Here, we show defective autophagy in Niemann-Pick type C1 (NPC1) disease associated with cholesterol accumulation, where the maturation of autophagosomes is impaired because of defective amphisome formation caused by failure in SNARE machinery, whereas the lysosomal proteolytic function remains unaffected. Expression of functional NPC1 protein rescues this defect. Inhibition of autophagy also causes cholesterol accumulation. Compromised autophagy was seen in disease-affected organs of Npc1 mutant mice. Of potential therapeutic relevance is that HP-β-cyclodextrin, which is used for cholesterol-depletion treatment, impedes autophagy, whereas stimulating autophagy restores its function independent of amphisome formation. Our data suggest that a low dose of HP-β-cyclodextrin that does not perturb autophagy, coupled with an autophagy inducer, may provide a rational treatment strategy for NPC1 disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy*
  • Cells, Cultured
  • Cholesterol / deficiency
  • Cholesterol / metabolism
  • HEK293 Cells
  • Humans
  • Lysosomes / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Neurons / drug effects
  • Neurons / metabolism
  • Niemann-Pick C1 Protein
  • Niemann-Pick Disease, Type C / genetics
  • Niemann-Pick Disease, Type C / metabolism*
  • Rats
  • SNARE Proteins / metabolism
  • beta-Cyclodextrins / pharmacology

Substances

  • Membrane Glycoproteins
  • NPC1 protein, rat
  • Niemann-Pick C1 Protein
  • SNARE Proteins
  • beta-Cyclodextrins
  • Cholesterol