Endogenous developmental endothelial locus-1 limits ischaemia-related angiogenesis by blocking inflammation

Thromb Haemost. 2017 Jun 2;117(6):1150-1163. doi: 10.1160/TH16-05-0354. Epub 2017 Apr 27.

Abstract

We have recently identified endothelial cell-secreted developmental endothelial locus-1 (Del-1) as an endogenous inhibitor of β2-integrin-dependent leukocyte infiltration. Del-1 was previously also implicated in angiogenesis. Here, we addressed the role of endogenously produced Del-1 in ischaemia-related angiogenesis. Intriguingly, Del-1-deficient mice displayed increased neovascularisation in two independent ischaemic models (retinopathy of prematurity and hind-limb ischaemia), as compared to Del-1-proficient mice. On the contrary, angiogenic sprouting in vitro or ex vivo (aortic ring assay) and physiological developmental retina angiogenesis were not affected by Del-1 deficiency. Mechanistically, the enhanced ischaemic neovascularisation in Del-1-deficiency was linked to higher infiltration of the ischaemic tissue by CD45+ haematopoietic and immune cells. Moreover, Del-1-deficiency promoted β2-integrin-dependent adhesion of haematopoietic cells to endothelial cells in vitro, and the homing of hematopoietic progenitor cells and of immune cell populations to ischaemic muscles in vivo. Consistently, the increased hind limb ischaemia-related angiogenesis in Del-1 deficiency was completely reversed in mice lacking both Del-1 and the β2-integrin LFA-1. Additionally, enhanced retinopathy-associated neovascularisation in Del-1-deficient mice was reversed by LFA-1 blockade. Our data reveal a hitherto unrecognised function of endogenous Del-1 as a local inhibitor of ischaemia-induced angiogenesis by restraining LFA-1-dependent homing of pro-angiogenic haematopoietic cells to ischaemic tissues. Our findings are relevant for the optimisation of therapeutic approaches in the context of ischaemic diseases.

Keywords: Angiogenesis; integrins; leukocytes.

MeSH terms

  • Animals
  • Calcium-Binding Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Adhesion
  • Cell Adhesion Molecules
  • Cell Movement
  • Disease Models, Animal
  • Endothelium, Vascular / physiology*
  • Extremities / pathology
  • Hematopoietic Stem Cells / physiology*
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Intercellular Signaling Peptides and Proteins
  • Ischemia / immunology
  • Ischemia / metabolism*
  • Leukocytes / physiology*
  • Lymphocyte Function-Associated Antigen-1 / genetics
  • Lymphocyte Function-Associated Antigen-1 / immunology
  • Lymphocyte Function-Associated Antigen-1 / metabolism
  • Mice
  • Mice, Knockout
  • Neovascularization, Physiologic
  • RNA, Small Interfering / genetics
  • Retinopathy of Prematurity / immunology
  • Retinopathy of Prematurity / metabolism*

Substances

  • Calcium-Binding Proteins
  • Carrier Proteins
  • Cell Adhesion Molecules
  • EDIL3 protein, human
  • Edil3 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Lymphocyte Function-Associated Antigen-1
  • RNA, Small Interfering