Intracellular accumulation of amyloidogenic fragments of amyloid-beta precursor protein in neurons with Niemann-Pick type C defects is associated with endosomal abnormalities

Am J Pathol. 2004 Mar;164(3):975-85. doi: 10.1016/s0002-9440(10)63185-9.

Abstract

Niemann-Pick type C disease (NPC) is characterized by neurodegeneration secondary to impaired cholesterol trafficking and excessive glycosphingolipid storage. Abnormal cholesterol and ganglioside metabolism may influence the generation and aggregation of amyloidogenic fragments (ie, C99 and Abeta) from amyloid-beta precursor protein (APP), crucial factors causing neurodegeneration in Alzheimer's disease. To reveal whether abnormal accumulation and aggregation of APP fragments also occurs in NPC, we studied their expression in cultured cortical neurons treated with U18666A, a compound widely used to induce NPC defects, and also in brain tissues from NPC patients. U18666A treatment resulted in increased intraneuronal levels of C99 and insoluble Abeta42, which were distributed among early and late endosomes, in compartments distinct from where endogenous cholesterol accumulates. Analyses of NPC brains revealed that C99 or other APP C-terminal fragments (APP-CTF), but not Abeta42, accumulated in Purkinje cells, mainly in early endosomes. In contrast, in hippocampal pyramidal neurons, the major accumulated species was Abeta42, in late endosomes. Similar to what has been shown in Alzheimer's disease, cathepsin D, a lysosomal hydrolase, was redistributed to early endosomes in NPC Purkinje cells, where it co-localized with C99/APP-CTF. Our results suggest that endosomal abnormalities related to abnormal lipid trafficking in NPC may contribute to abnormal APP processing and Abeta42/C99/APP-CTF deposition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Amyloid beta-Protein Precursor / drug effects
  • Amyloid beta-Protein Precursor / metabolism*
  • Androstenes / pharmacology
  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Cathepsin D / metabolism
  • Cells, Cultured
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Child
  • Child, Preschool
  • Endosomes / drug effects
  • Endosomes / metabolism
  • Endosomes / pathology*
  • Enzyme Inhibitors / pharmacology
  • Enzyme-Linked Immunosorbent Assay
  • Humans
  • Immunohistochemistry
  • Inclusion Bodies / drug effects
  • Inclusion Bodies / metabolism
  • Inclusion Bodies / pathology
  • Infant
  • Mice
  • Middle Aged
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / pathology*
  • Niemann-Pick Diseases / metabolism
  • Niemann-Pick Diseases / pathology*
  • Peptide Fragments / metabolism
  • Protein Transport

Substances

  • Amyloid beta-Protein Precursor
  • Androstenes
  • Enzyme Inhibitors
  • Peptide Fragments
  • amyloid precursor protein carboxyl-terminal fragment gamma
  • 3-beta-(2-(diethylamino)ethoxy)androst-5-en-17-one
  • Cathepsin D