Contribution of bone marrow-derived cells associated with brain angiogenesis is primarily through leukocytes and macrophages

Arterioscler Thromb Vasc Biol. 2008 Dec;28(12):2151-7. doi: 10.1161/ATVBAHA.108.176297. Epub 2008 Sep 18.

Abstract

Objective: We investigated the role of bone marrow-derived cells (BMDCs) in an angiogenic focus, induced by VEGF stimulation.

Methods and results: BM from GFP donor mice was isolated and transplanted into lethally irradiated recipients. Four weeks after transplantation, groups of mice received adeno-associated viral vector (AAV)-VEGF or AAV-lacZ gene (control) injection and were euthanized at 1 to 24 weeks. BMDCs were characterized by double-labeled immunostaining. The function of BMDCs was further examined through matrix metalloproteinase (MMP)-2 and -9 activity. We found that capillary density increased after 2 weeks, peaked at 4 weeks (P<0.01), and sustained up to 24 weeks after gene transfer. GFP-positive BMDCs infiltration in the angiogenic focus began at 1 week, peaked at 2 weeks, and decreased thereafter. The GFP-positive BMDCs were colocalized with CD45 (94%), CD68 (71%), 5% Vimentin (5%), CD31/von Willebrand factor (vWF) (1%), and alpha-smooth muscle actin (alpha -SMA, 0.5%). Infiltrated BMDCs expressed MMP-9. MMP-9 KO mice confirmed the dependence of the angiogenic response on MMP-9 availability.

Conclusions: Nearly all BMDCs in the angiogenic focus showed expression for leukocytes/macrophages, indicating that BMDCs minimally incorporated into the neovasculature. Colocalization of MMPs with GFP suggests that BMDCs play a critical role in VEGF-induced angiogenic response through up-regulation of MMPs.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Blood-Brain Barrier / physiology
  • Bone Marrow Cells / cytology*
  • Bone Marrow Cells / metabolism
  • Bone Marrow Transplantation
  • Brain / blood supply*
  • Brain / cytology*
  • Dependovirus / genetics
  • Green Fluorescent Proteins / genetics
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • Leukocytes / cytology
  • Leukocytes / metabolism
  • Macrophages / cytology
  • Macrophages / metabolism
  • Male
  • Matrix Metalloproteinase 9 / deficiency
  • Matrix Metalloproteinase 9 / genetics
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Neovascularization, Physiologic*
  • Recombinant Proteins / genetics
  • Transduction, Genetic
  • Vascular Endothelial Growth Factor A / genetics

Substances

  • Icam1 protein, mouse
  • Recombinant Proteins
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • enhanced green fluorescent protein
  • Intercellular Adhesion Molecule-1
  • Green Fluorescent Proteins
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse