Vulnerability to shear stress caused by altered peri-endothelial matrix is a key feature of Moyamoya disease

Sci Rep. 2021 Jan 15;11(1):1552. doi: 10.1038/s41598-021-81282-9.

Abstract

Moyamoya disease (MMD) is characterized by progressive bilateral stenotic changes in the terminal portion of the internal carotid arteries. Although RNF213 was identified as a susceptibility gene for MMD, the exact pathogenesis remains unknown. Immunohistochemical analysis of autopsy specimens from a patient with MMD revealed marked accumulation of hyaluronan and chondroitin sulfate (CS) in the thickened intima of occlusive lesions of MMD. Hyaluronan synthase 2 was strongly expressed in endothelial progenitor cells in the thickened intima. Furthermore, MMD lesions showed minimal staining for CS and hyaluronan in the endothelium, in contrast to control endothelium showing positive staining for both. Glycosaminoglycans of endothelial cells derived from MMD and control induced pluripotent stem cells demonstrated a decreased amount of CS, especially sulfated CS, in MMD. A computational fluid dynamics model showed highest wall shear stress values in the terminal portion of the internal carotid artery, which is the predisposing region in MMD. Because the peri-endothelial extracellular matrix plays an important role in protection, cell adhesion and migration, an altered peri-endothelial matrix in MMD may contribute to endothelial vulnerability to wall shear stress. Invading endothelial progenitor cells repairing endothelial injury would produce excessive hyaluronan and CS in the intima, and cause vascular stenosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / metabolism
  • Adolescent
  • Aged
  • Biomechanical Phenomena / physiology
  • Carotid Artery, Internal / pathology
  • Carotid Intima-Media Thickness
  • Chondroitin Sulfates / analysis
  • Endothelial Cells / metabolism*
  • Endothelial Cells / physiology
  • Endothelium / metabolism
  • Female
  • Genetic Predisposition to Disease
  • Humans
  • Hyaluronic Acid / analysis
  • Hydrodynamics
  • Induced Pluripotent Stem Cells / metabolism
  • Male
  • Moyamoya Disease / metabolism
  • Moyamoya Disease / physiopathology*
  • Shear Strength / physiology
  • Stress, Mechanical
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Hyaluronic Acid
  • Chondroitin Sulfates
  • RNF213 protein, human
  • Ubiquitin-Protein Ligases
  • Adenosine Triphosphatases