Methyl-β-cyclodextrin restores impaired autophagy flux in Niemann-Pick C1-deficient cells through activation of AMPK

Autophagy. 2017 Aug 3;13(8):1435-1451. doi: 10.1080/15548627.2017.1329081. Epub 2017 Jun 14.

Abstract

The drug 2-hydroxypropyl-β-cyclodextrin (HPβCD) reduces lysosomal cholesterol accumulation in Niemann-Pick disease, type C (NPC) and has been advanced to human clinical trials. However, its mechanism of action for reducing cholesterol accumulation in NPC cells is uncertain and its molecular target is unknown. We found that methyl-β-cyclodextrin (MβCD), a potent analog of HPβCD, restored impaired macroautophagy/autophagy flux in Niemann-Pick disease, type C1 (NPC1) cells. This effect was mediated by a direct activation of AMP-activated protein kinase (AMPK), an upstream kinase in the autophagy pathway, through MβCD binding to its β-subunits. Knockdown of PRKAB1 or PRKAB2 (encoding the AMPK β1 or β2 subunit) expression and an AMPK inhibitor abolished MβCD-mediated reduction of cholesterol storage in NPC1 cells. The results demonstrate that AMPK is the molecular target of MβCD and its activation enhances autophagy flux, thereby mitigating cholesterol accumulation in NPC1 cells. The results identify AMPK as an attractive target for drug development to treat NPC.

Keywords: AMPK; Niemann-Pick disease type C; autophagy flux; drug development; methyl-β-cyclodextrin; molecular target.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism*
  • Autophagosomes / drug effects
  • Autophagosomes / metabolism
  • Autophagy* / drug effects
  • Boron Compounds / metabolism
  • Cholesterol / metabolism
  • Endocytosis / drug effects
  • Enzyme Activation / drug effects
  • Enzyme Activators / pharmacology
  • Humans
  • Kinetics
  • Models, Biological
  • Niemann-Pick Disease, Type C / drug therapy*
  • Niemann-Pick Disease, Type C / enzymology
  • Niemann-Pick Disease, Type C / pathology*
  • Protein Kinase Inhibitors / pharmacology
  • beta-Cyclodextrins / pharmacology
  • beta-Cyclodextrins / therapeutic use*

Substances

  • 4,4-difluoro-4-bora-3a,4a-diaza-s-indacene
  • Boron Compounds
  • Enzyme Activators
  • Protein Kinase Inhibitors
  • beta-Cyclodextrins
  • methyl-beta-cyclodextrin
  • Cholesterol
  • AMP-Activated Protein Kinases