proBDNF is modified by advanced glycation end products in Alzheimer's disease and causes neuronal apoptosis by inducing p75 neurotrophin receptor processing

Mol Brain. 2018 Nov 14;11(1):68. doi: 10.1186/s13041-018-0411-6.

Abstract

Alzheimer disease (AD) is a complex pathology related to multiple causes including oxidative stress. Brain-derived neurotrophic factor (BDNF) is a neutrotrophic factor essential for the survival and differentiation of neurons and is considered a key target in the pathophysiology of various neurodegenerative diseases, as for example AD. Contrarily to BDNF, the precursor form of BDNF (proBDNF) induces apoptosis through the specific interaction with p75 and its co-receptor, Sortilin.We used hippocampal tissue and cerebrospinal fluid from AD patients and controls. to study the localization and the levels of proBDNF, p75 and Sortilin as well as the post-traduccional modifications of proBDNF induced by Radical Oxygen Species, by immunofluorescence and Western blot. Differentiation and survival were assessed on differentiated mouse hippocampal neurons derived from postnatal neural stem cells from WT animals or from the transgenic AD animal model APP/PS1∆E9, based on mutations of familiar AD. In AD patients we observe a significative increase of proBDNF and Sortilin expression and a significative increase of the ratio proBDNF/BDNF in their cerebrospinal fluid compared to controls. In addition, the proBDNF of AD patients is modified by ROS-derived advanced glycation end products, which prevent the processing of the proBDNF to the mature BDNF, leading to an increase of pathogenicity and a decrease of trophic effects. The cerebrospinal fluid from AD patients, but not from controls, induces apoptosis in differentiated hippocampal neurons mainly by the action of AGE-modified proBDNF present in the cerebrospinal fluid of the patients. This effect is triggered by the activation and processing of p75 that stimulate the internalization of the intracellular domain (ICD) within the nucleus causing apoptosis. Induction of apoptosis and p75 ICD internalization by AD patients-derived proBDNF is further enhanced in neuron cultures from the AD model expressing the APP/PS1∆E9 transgene.Our results indicate the importance of proBDNF neurotoxic signaling in AD pathology essentially by three mechanisms: i) by an increase of proBDNF stability due to ROS-induced post-traductional modifications; ii) by the increase of expression of the p75 co-receptor, Sortilin and iii) by the increase of the basal levels of p75 processing found in AD.

Keywords: Alzheimer’s disease; BDNF; Biomarkers; Oxidative stress; Sortilin; p75; proBDNF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Vesicular Transport / metabolism
  • Aged
  • Aged, 80 and over
  • Alzheimer Disease / cerebrospinal fluid
  • Alzheimer Disease / metabolism*
  • Alzheimer Disease / pathology*
  • Animals
  • Apoptosis* / drug effects
  • Brain-Derived Neurotrophic Factor / metabolism*
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • Female
  • Glycation End Products, Advanced / metabolism*
  • Hippocampus / metabolism
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Middle Aged
  • Mutation / genetics
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / pathology*
  • Protein Processing, Post-Translational* / drug effects
  • Pyruvaldehyde / pharmacology
  • Receptor, Nerve Growth Factor / metabolism*
  • Young Adult

Substances

  • Adaptor Proteins, Vesicular Transport
  • Brain-Derived Neurotrophic Factor
  • Glycation End Products, Advanced
  • Receptor, Nerve Growth Factor
  • Pyruvaldehyde
  • sortilin