Multimodal mass spectrometry imaging for plaque- and region-specific neurolipidomics in Alzheimer's disease mouse models

Nat Commun. 2025 Dec 9;16(1):10969. doi: 10.1038/s41467-025-65956-w.

Abstract

The progressive accumulation of amyloid beta (Aβ) plaques is a hallmark of Alzheimer's disease (AD). However, the biochemical mechanisms of their formation and the consequences associated with plaque formation remain elusive. In female 5xFAD and APPNL-G-F mice, we map region-specific, plaque-associated lipids with large molecular coverage including isomers. We describe a multimodal framework that integrates matrix assisted laser desorption/ionization with laser-induced postionization (MALDI-2) mass spectrometry imaging, trapped ion mobility spectrometry, and fluorescence microscopy. Our approach improves detectability and spatial-chemical resolution. We couple these measurements with a computational pipeline for multimodal image coregistration and discovery of plaque-altered lipids. Here, we show the lipids in and around Aβ plaques are highly heterogeneous. Integration of our data with existing spatial transcriptomics data suggests that region-specific accumulation of simple gangliosides is likely driven by lysosomal degradation of complex species. Together, this work provides a generalizable framework to understand lipid alterations within the Aβ plaque microenvironment.

MeSH terms

  • Alzheimer Disease* / diagnostic imaging
  • Alzheimer Disease* / genetics
  • Alzheimer Disease* / metabolism
  • Alzheimer Disease* / pathology
  • Amyloid beta-Peptides / metabolism
  • Animals
  • Brain* / diagnostic imaging
  • Brain* / metabolism
  • Brain* / pathology
  • Disease Models, Animal
  • Female
  • Humans
  • Lipid Metabolism
  • Lipids / analysis
  • Lipids / chemistry
  • Mice
  • Mice, Transgenic
  • Microscopy, Fluorescence
  • Multimodal Imaging* / methods
  • Plaque, Amyloid* / diagnostic imaging
  • Plaque, Amyloid* / metabolism
  • Plaque, Amyloid* / pathology
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization / methods

Substances

  • Amyloid beta-Peptides
  • Lipids