Proteomics Time-Course Study of App Knock-In Mice Reveals Novel Presymptomatic Aβ42-Induced Pathways to Alzheimer's Disease Pathology

J Alzheimers Dis. 2020;75(1):321-335. doi: 10.3233/JAD-200028.

Abstract

Background: The 42 amino acids long amyloid-β peptide, Aβ42, may initiate a cascade of events leading to the severe neurodegeneration observed in Alzheimer's disease (AD) brain. However, the underlying molecular mechanisms remain to be established.

Objective: To find early Aβ42-induced AD related mechanisms, we performed a brain proteomics time-course study on a novel App knock-in AD mouse model, AppNL-F, expressing high levels of Aβ42 without AβPP overexpression artifacts.

Methods: Hippocampus and cortex were analyzed separately by using 18O-labelling mass spectrometry to reveal alterations in protein levels. Pathway analysis of proteomics data was used to identify altered biological functions. Immunohistochemistry was used to further investigate a significant key regulatory protein.

Results: Around 100 proteins were differently expressed in AppNL-F mice at each time point (3, 6, 9, and 18 months of age) as compared to wild type mice. Strikingly, already at 3 months of age-long before Aβ plaque development and memory impairment-several pathways, including long-term potentiation and synaptic plasticity, were downregulated, and neuritogenesis was increased. Huntingtin (HTT) was identified as an upstream regulator, i.e., a key protein affecting the levels of several proteins. Increased levels of HTT in hippocampus of AppNL-F mice was supported by immunofluorescence microscopy.

Conclusion: Notably, the proteome was significantly altered already at 3 months of age, 6 months before the development of plaques. Differentially expressed proteins varied over time, indicating that increased Aβ42 levels initiate a cascade of events that eventually manifests in amyloid depositions, inflammation, and decline in memory.

Keywords: Alzheimer’s disease; App knock-in mouse model; amyloid-β; ingenuity pathway analysis; proteomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / genetics*
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Amyloid beta-Protein Precursor / genetics*
  • Amyloid beta-Protein Precursor / metabolism
  • Animals
  • Cerebral Cortex / metabolism*
  • Cerebral Cortex / pathology
  • Disease Models, Animal
  • Down-Regulation
  • Gene Knock-In Techniques
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Huntingtin Protein / genetics
  • Huntingtin Protein / metabolism
  • Mass Spectrometry
  • Mice
  • Mice, Transgenic
  • Proteome / metabolism*

Substances

  • Amyloid beta-Protein Precursor
  • Huntingtin Protein
  • Proteome