Post-stroke hippocampal neurogenesis is impaired by microvascular dysfunction and PI3K signaling in cerebral amyloid angiopathy

Cell Rep. 2024 Oct 22;43(10):114848. doi: 10.1016/j.celrep.2024.114848. Epub 2024 Oct 10.

Abstract

Ischemic stroke and cerebral amyloid angiopathy (CAA) pose significant challenges in an aging population, particularly in post-stroke recovery. Using the 5xFAD mouse model, we explore the relationship between CAA, ischemic stroke, and tissue recovery. We hypothesize that amyloid-beta accumulation worsens stroke outcomes by inducing blood-brain barrier (BBB) dysfunction, leading to impaired neurogenesis. Our findings show that CAA exacerbates stroke outcomes, with mice exhibiting constricted BBB microvessels, reduced cerebral blood flow, and impaired tissue recovery. Transcriptional analysis shows that endothelial cells and neural progenitor cells (NPCs) in the hippocampus exhibit differential gene expression in response to CAA and stroke, specifically targeting the phosphatidylinositol 3-kinase (PI3K) pathway. In vitro experiments with human NPCs validate these findings, showing that disruption of the CXCL12-PIK3C2A-CREB3L2 axis impairs neurogenesis. Notably, PI3K pathway activation restores neurogenesis, highlighting a potential therapeutic approach. These results suggest that CAA combined with stroke induces microvascular dysfunction and aberrant neurogenesis through this specific pathway.

Keywords: CAA; CP: Cell biology; CP: Neuroscience; PI3K; hippocampus; neurogenesis; stroke.

MeSH terms

  • Animals
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology
  • Cerebral Amyloid Angiopathy* / metabolism
  • Cerebral Amyloid Angiopathy* / pathology
  • Chemokine CXCL12 / metabolism
  • Disease Models, Animal
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Hippocampus* / metabolism
  • Hippocampus* / pathology
  • Humans
  • Male
  • Mice
  • Microvessels* / metabolism
  • Microvessels* / pathology
  • Neural Stem Cells / metabolism
  • Neurogenesis*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Signal Transduction*
  • Stroke* / metabolism
  • Stroke* / pathology
  • Stroke* / physiopathology

Substances

  • Chemokine CXCL12
  • Phosphatidylinositol 3-Kinases