Endoglin deficiency in bone marrow is sufficient to cause cerebrovascular dysplasia in the adult mouse after vascular endothelial growth factor stimulation

Stroke. 2013 Mar;44(3):795-8. doi: 10.1161/STROKEAHA.112.671974. Epub 2013 Jan 10.

Abstract

Background and purpose: Bone marrow-derived cells (BMDCs) home to vascular endothelial growth factor (VEGF)-induced brain angiogenic foci, and VEGF induces cerebrovascular dysplasia in adult endoglin heterozygous (Eng(+/-)) mice. We hypothesized that Eng(+/-) BMDCs cause cerebrovascular dysplasia in the adult mouse after VEGF stimulation.

Methods: BM transplantation was performed using adult wild-type (WT) and Eng(+/-) mice as donors/recipients. An adeno-associated viral vector expressing VEGF was injected into the basal ganglia 4 weeks after transplantation. Vascular density, dysplasia index (vessels >15 µm/100 vessels), and BMDCs in the angiogenic foci were analyzed.

Results: The dysplasia index of WT/Eng(+/-) BM mice was higher than WT/WT BM mice (P<0.001) and was similar to Eng(+/-)/Eng(+/-) BM mice (P=0.2). Dysplasia in Eng(+/-) mice was partially rescued by WT BM (P<0.001). WT/WT BM and WT/Eng(+/-) BM mice had similar numbers of BMDCs in the angiogenic foci (P=0.4), most of which were CD68(+). Eng(+/-) monocytes/macrophages expressed less matrix metalloproteinase-9 and Notch1.

Conclusions: Endoglin-deficient BMDCs are sufficient for VEGF to induce vascular dysplasia in the adult mouse brain. Our data support a previously unrecognized role of BM in the development of cerebrovascular malformations.

MeSH terms

  • Animals
  • Bone Marrow / metabolism*
  • Bone Marrow Transplantation
  • Cerebrovascular Disorders / chemically induced*
  • Endoglin
  • Intracellular Signaling Peptides and Proteins / deficiency*
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Macrophages / metabolism
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Knockout
  • Models, Animal
  • Monocytes / metabolism
  • Receptor, Notch1 / metabolism
  • Vascular Endothelial Growth Factor A / adverse effects*
  • Vascular Endothelial Growth Factor A / pharmacology
  • Vascular Malformations / chemically induced*

Substances

  • Endoglin
  • Eng protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Notch1 protein, mouse
  • Receptor, Notch1
  • Vascular Endothelial Growth Factor A
  • Matrix Metalloproteinase 9