Molecular determinants of phospholipid treatment to reduce intracellular cholesterol accumulation in NPC1 deficiency

J Biol Chem. 2024 Nov;300(11):107889. doi: 10.1016/j.jbc.2024.107889. Epub 2024 Oct 11.

Abstract

Niemann-Pick type C (NPC) disease, caused by mutations in the NPC1 or NPC2 genes, leads to abnormal intracellular cholesterol accumulation in late endosomes/lysosomes. Exogenous enrichment with lysobisphosphatidic acid (LBPA), also known as bis-monoacylglycerol phosphate, either directly or via the LBPA precursor phosphatidylglycerol (PG), has been investigated as a therapeutic intervention to reduce cholesterol accumulation in NPC disease. Here, we report the effects of stereoisomer configuration and acyl chain composition of LBPA on cholesterol clearance in NPC1-deficient cells. We find that S,R, S,S, and S,R LBPA stereoisomers behaved similarly, with all 3 compounds leading to comparable reductions in filipin staining in two NPC1-deficient human fibroblast cell lines. Examination of several LBPA molecular species containing one or two monounsaturated or polyunsaturated acyl chains showed that all LBPA species containing one 18:1 chain significantly reduced cholesterol accumulation, whereas the shorter chain species di-14:0 LBPA had little effect on cholesterol clearance in NPC1-deficient cells. Since cholesterol accumulation in NPC1-deficient cells can also be cleared by PG incubation, we used nonhydrolyzable PG analogs to determine whether conversion to LBPA is required for sterol clearance, or whether PG itself is effective. The results showed that nonhydrolyzable PG species were not appreciably converted to LBPA and showed virtually no cholesterol clearance efficacy in NPC1-deficient cells, supporting the notion that LBPA is the active agent promoting late endosome/lysosome cholesterol clearance. Overall these studies are helping to define the molecular requirements for potential therapeutic use of LBPA as an option for addressing NPC disease.

Keywords: Niemann-Pick C disease; bis-monoacylglycerol phosphate; cholesterol; lysobisphosphatidic acid; lysosome; phosphatidylglycerol; phospholipid.

MeSH terms

  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Line
  • Cholesterol* / metabolism
  • Endosomes / metabolism
  • Fibroblasts* / drug effects
  • Fibroblasts* / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins* / genetics
  • Intracellular Signaling Peptides and Proteins* / metabolism
  • Lysophospholipids* / metabolism
  • Lysosomes / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Monoglycerides* / metabolism
  • Niemann-Pick C1 Protein*
  • Niemann-Pick Disease, Type C* / drug therapy
  • Niemann-Pick Disease, Type C* / genetics
  • Niemann-Pick Disease, Type C* / metabolism
  • Niemann-Pick Disease, Type C* / pathology

Substances

  • Cholesterol
  • Niemann-Pick C1 Protein
  • NPC1 protein, human
  • bis(monoacylglyceryl)phosphate
  • Intracellular Signaling Peptides and Proteins
  • Lysophospholipids
  • Monoglycerides
  • Carrier Proteins
  • Membrane Glycoproteins