Monomeric C-reactive protein via endothelial CD31 for neurovascular inflammation in an ApoE genotype-dependent pattern: A risk factor for Alzheimer's disease?

Aging Cell. 2021 Nov;20(11):e13501. doi: 10.1111/acel.13501. Epub 2021 Oct 23.

Abstract

In chronic peripheral inflammation, endothelia in brain capillary beds could play a role for the apolipoprotein E4 (ApoE4)-mediated risk for Alzheimer's disease (AD) risk. Using human brain tissues, here we demonstrate that the interactions of endothelial CD31 with monomeric C-reactive protein (mCRP) versus ApoE were linked with shortened neurovasculature for AD pathology and cognition. Using ApoE knock-in mice, we discovered that intraperitoneal injection of mCRP, via binding to CD31 on endothelial surface and increased CD31 phosphorylation (pCD31), leading to cerebrovascular damage and the extravasation of T lymphocytes into the ApoE4 brain. While mCRP was bound to endothelial CD31 in a dose- and time-dependent manner, knockdown of CD31 significantly decreased mCRP binding and altered the expressions of vascular-inflammatory factors including vWF, NF-κB and p-eNOS. RNAseq revealed endothelial pathways related to oxidative phosphorylation and AD pathogenesis were enhanced, but endothelial pathways involving in epigenetics and vasculogenesis were inhibited in ApoE4. This is the first report providing some evidence on the ApoE4-mCRP-CD31 pathway for the cross talk between peripheral inflammation and cerebrovasculature leading to AD risk.

Keywords: Alzheimer’s disease (AD); Apolipoprotein E; CD31; cerebrovascular; endothelia; lymphocyte extravasation; monomeric C-reactive protein; neuroinflammation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism*
  • Alzheimer Disease / pathology
  • Animals
  • Apolipoprotein E4 / metabolism
  • Apolipoproteins E / genetics
  • Apolipoproteins E / metabolism*
  • Brain / metabolism
  • C-Reactive Protein / administration & dosage
  • C-Reactive Protein / metabolism*
  • Case-Control Studies
  • Cells, Cultured
  • Endothelial Cells / metabolism*
  • Female
  • Gene Knock-In Techniques
  • Gene Knockdown Techniques
  • Genotype*
  • Humans
  • Inflammation / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout, ApoE
  • Middle Aged
  • Oxidative Phosphorylation / drug effects
  • Platelet Endothelial Cell Adhesion Molecule-1 / genetics
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism*
  • Risk Factors
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*

Substances

  • ApoE protein, human
  • Apoe protein, mouse
  • Apolipoprotein E4
  • Apolipoproteins E
  • PECAM1 protein, human
  • Pecam1 protein, mouse
  • Platelet Endothelial Cell Adhesion Molecule-1
  • C-Reactive Protein