Endothelial cell-derived pentraxin 3 limits the vasoreparative therapeutic potential of circulating angiogenic cells

Cardiovasc Res. 2016 Dec;112(3):677-688. doi: 10.1093/cvr/cvw209. Epub 2016 Sep 22.

Abstract

Aims: Circulating angiogenic cells (CACs) promote revascularization of ischaemic tissues although their underlying mechanism of action and the consequences of delivering varying number of these cells for therapy remain unknown. This study investigates molecular mechanisms underpinning CAC modulation of blood vessel formation.

Methods and results: CACs at low (2 × 105 cells/mL) and mid (2 × 106 cells/mL) cellular densities significantly enhanced endothelial cell tube formation in vitro, while high density (HD) CACs (2 × 107 cells/mL) significantly inhibited this angiogenic process. In vivo, Matrigel-based angiogenesis assays confirmed mid-density CACs as pro-angiogenic and HD CACs as anti-angiogenic. Secretome characterization of CAC-EC conditioned media identified pentraxin 3 (PTX3) as only present in the HD CAC-EC co-culture. Recombinant PTX3 inhibited endothelial tube formation in vitro and in vivo. Importantly, our data revealed that the anti-angiogenic effect observed in HD CAC-EC co-cultures was significantly abrogated when PTX3 bioactivity was blocked using neutralizing antibodies or PTX3 siRNA in endothelial cells. We show evidence for an endothelial source of PTX3, triggered by exposure to HD CACs. In addition, we confirmed that PTX3 inhibits fibroblast growth factor (FGF) 2-mediated angiogenesis, and that the PTX3 N-terminus, containing the FGF-binding site, is responsible for such anti-angiogenic effects.

Conclusion: Endothelium, when exposed to HD CACs, releases PTX3 which markedly impairs the vascular regenerative response in an autocrine manner. Therefore, CAC density and accompanying release of angiocrine PTX3 are critical considerations when using these cells as a cell therapy for ischaemic disease.

Keywords: Cell therapy; Circulating angiogenic cell; Ischaemia; PTX3; Vascular repair.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Autocrine Communication
  • C-Reactive Protein / chemistry
  • C-Reactive Protein / genetics
  • C-Reactive Protein / metabolism*
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / metabolism
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Endothelial Progenitor Cells / metabolism*
  • Endothelial Progenitor Cells / transplantation
  • Fibroblast Growth Factor 2 / metabolism
  • Humans
  • Inflammation Mediators / metabolism
  • Mice
  • Mice, Nude
  • Middle Aged
  • Neovascularization, Physiologic*
  • Oxygen
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • RNA Interference
  • Retinal Neovascularization
  • Retinopathy of Prematurity / metabolism
  • Retinopathy of Prematurity / physiopathology
  • Retinopathy of Prematurity / surgery
  • Serum Amyloid P-Component / chemistry
  • Serum Amyloid P-Component / genetics
  • Serum Amyloid P-Component / metabolism*
  • Signal Transduction
  • Transfection
  • Young Adult

Substances

  • Cytokines
  • Inflammation Mediators
  • Serum Amyloid P-Component
  • Fibroblast Growth Factor 2
  • PTX3 protein
  • C-Reactive Protein
  • Oxygen