Niemann-Pick Type C Disease Reveals a Link between Lysosomal Cholesterol and PtdIns(4,5)P2 That Regulates Neuronal Excitability

Cell Rep. 2019 May 28;27(9):2636-2648.e4. doi: 10.1016/j.celrep.2019.04.099.

Abstract

There is increasing evidence that the lysosome is involved in the pathogenesis of a variety of neurodegenerative disorders. Thus, mechanisms that link lysosome dysfunction to the disruption of neuronal homeostasis offer opportunities to understand the molecular underpinnings of neurodegeneration and potentially identify specific therapeutic targets. Here, using a monogenic neurodegenerative disorder, NPC1 disease, we demonstrate that reduced cholesterol efflux from lysosomes aberrantly modifies neuronal firing patterns. The molecular mechanism linking alterations in lysosomal cholesterol egress to intrinsic tuning of neuronal excitability is a transcriptionally mediated upregulation of the ABCA1 transporter, whose PtdIns(4,5)P2-floppase activity decreases plasma membrane PtdIns(4,5)P2. The consequence of reduced PtdIns(4,5)P2 is a parallel decrease in a key regulator of neuronal excitability, the voltage-gated KCNQ2/3 potassium channel, which leads to hyperexcitability in NPC1 disease neurons. Thus, cholesterol efflux from lysosomes regulates PtdIns(4,5)P2 to shape the electrical and functional identity of the plasma membrane of neurons in health and disease.

Keywords: ABCA1; KCNQ2/3 channels; NPC1; NPC1 disease; PtdIns(4,5)P(2); cholesterol; excitability; neurodegeneration; phosphoinositides.

Publication types

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

MeSH terms

  • ATP Binding Cassette Transporter 1 / genetics
  • ATP Binding Cassette Transporter 1 / metabolism
  • Animals
  • Biological Transport
  • Cell Membrane / metabolism*
  • Cholesterol / metabolism*
  • Female
  • Intracellular Signaling Peptides and Proteins / physiology*
  • KCNQ2 Potassium Channel / genetics
  • KCNQ2 Potassium Channel / metabolism
  • KCNQ3 Potassium Channel / genetics
  • KCNQ3 Potassium Channel / metabolism
  • Lysosomes / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons / cytology
  • Neurons / physiology*
  • Niemann-Pick C1 Protein
  • Niemann-Pick Disease, Type C / metabolism
  • Niemann-Pick Disease, Type C / physiopathology*
  • Phosphatidylinositol 4,5-Diphosphate / metabolism*

Substances

  • ABCA1 protein, mouse
  • ATP Binding Cassette Transporter 1
  • Intracellular Signaling Peptides and Proteins
  • KCNQ2 Potassium Channel
  • KCNQ3 Potassium Channel
  • Kcnq2 protein, mouse
  • Kcnq3 protein, mouse
  • Nerve Tissue Proteins
  • Niemann-Pick C1 Protein
  • Npc1 protein, mouse
  • Phosphatidylinositol 4,5-Diphosphate
  • Cholesterol