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Basic Science and Pathogenesis.

Katherine M Sheu1, Mitchell H Murdock1, Na Sun1

  • 1Massachusetts Institute of Technology, Cambridge, MA, USA.

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Summary
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Alzheimer's disease (AD) progression impairs meningeal immune cell function, specifically reducing antigen presentation in endothelial cells and macrophages. This dysfunction in the brain's protective layers mirrors changes in brain tissue, suggesting new therapeutic targets.

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Area of Science:

  • Neuroimmunology
  • Molecular Psychiatry
  • Cellular Neuroscience

Background:

  • The meninges act as a critical interface regulating brain fluid, protein, and immune cell traffic.
  • Dysfunction of this neurovascular-immune interface is implicated in Alzheimer's Disease (AD) pathogenesis.
  • The specific roles of meningeal cell types in AD progression remain largely unknown.

Purpose of the Study:

  • To investigate the transcriptomic profiles of leptomeningeal cells in individuals with varying degrees of Alzheimer's pathology.
  • To identify how different meningeal cell types contribute to neuroinflammation and disease progression in AD.

Main Methods:

  • Single nuclei transcriptomic profiling of leptomeninges from 51 individuals.
  • Analysis of matched prefrontal cortex samples from 22 patients.
  • Identification of fibroblasts, vascular cells (endothelial, smooth muscle), and immune cells (macrophages, lymphocytes).

Main Results:

  • Increased AD pathology correlates with downregulated antigen presentation gene programs in meningeal endothelial cells and macrophages.
  • A similar decrease in antigen presentation was observed in the brain parenchyma of patients with high amyloid/tau burden.
  • Fibroblasts, endothelial cells, smooth muscle cells, macrophages, and lymphocytes were identified within the leptomeninges.

Conclusions:

  • Leptomeningeal and brain parenchymal dysfunction of humoral immunity are linked to worsening AD pathology.
  • These findings highlight a potential therapeutic target for systemic immune interventions in Alzheimer's Disease.
  • The study reveals a coordinated immune dysfunction across the brain-meningeal barrier in AD.