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Targeting VEGFR1 on endothelial progenitors modulates their differentiation potential

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Abstract

Objectives

We studied whether plasma levels of angiogenic factors VEGF and placental growth factor (PlGF) in coronary artery disease patients or undergoing cardiac surgery are modified, and whether those factors modulate endothelial progenitor’s angiogenic potential.

Methods and results

A total of 143 patients’ plasmas from two different studies were analyzed (30 coronary artery disease patients, 30 patients with stable angina, coupled with 30 age and sex-matched controls; 53 patients underwent cardiac surgery). Among factors screened, only PlGF was found significantly increased in these pathological populations. PlGF-1 and PlGF-2 were then tested on human endothelial-colony-forming cells (ECFCs). We found that PlGF-1 and PlGF-2 induce VEGFR1 phosphorylation and potentiate ECFCs tubulogenesis in vitro. ECFCs VEGFR1 was further inhibited using a specific small interfering RNA (siRNA) and the chemical compound 4321. We then observed that the VEGFR1-siRNA and the compound 4321 decrease ECFCs tubulogenesis potential in vitro. Finally, we tested the compound 4321 in the preclinical Matrigel®-plug model with C57Bl/6J mice as well as in the murine hindlimb ischemia model. We found that 4321 inhibited the plug vascularization, attested by the hemoglobin content and the VE-Cadherin expression level and that 4321 inhibited the post-ischemic revascularization.

Conclusion

PlGF plasma levels were found increased in cardiovascular patients. Disrupting PlGF/VEGFR1 pathway could modulate ECFC-induced tubulogenesis, the cell type responsible for newly formed vessels in vivo.

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Acknowledgments

We thank Anna Lokajczyk, Isabelle Galy-Fauroux and Berengere Marsac for their technical assistance in ECFCs culture, and IMTCE animal facilities (Paris Descartes University). We are indebted to the nursing services of Hôpital des Diaconnesses (Paris) and Hôpital des Instructions et des Armées de Begin (Saint Mandé) for providing umbilical cord blood samples. This work was supported by research grants from the Leducq TransAtlantic Network of Excellence on Atherothrombosis Research (Grant 04CVD01). Clément d’Audigier and Alexi Yon were supported by research grants from Fondation pour la Recherche Médicale.

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Authors and Affiliations

  1. Sorbonne Paris Cité, Université Paris Descartes, Paris, France

    Clément d’Audigier, Benoit Gautier, Alexis Yon, Jean-Meidi Alili, Coralie L. Guérin, Solène M. Evrard, Anne Godier, Skerdi Haviari, Marie Reille-Serroussi, Florent Huguenot, Blandine Dizier, Catherine Boisson-Vidal, Michel Vidal, Pascale Gaussem & David M. Smadja

  2. INSERM UMR-S 765, UFR des Sciences Pharmaceutiques et Biologiques, Paris, France

    Clément d’Audigier, Alexis Yon, Jean-Meidi Alili, Coralie L. Guérin, Solène M. Evrard, Anne Godier, Skerdi Haviari, Blandine Dizier, Catherine Boisson-Vidal, Pascale Gaussem & David M. Smadja

  3. Service d’hématologie biologique, AP-HP, Hôpital Européen Georges Pompidou, Paris, France

    Clément d’Audigier, Solène M. Evrard, Pascale Gaussem & David M. Smadja

  4. CNRS UMR 8638, UFR des Sciences Pharmaceutiques et Biologiques, Paris, France

    Benoit Gautier, Marie Reille-Serroussi, Florent Huguenot & Michel Vidal

  5. Service d`anesthésie et réanimation, AP-HP, Hôpital Cochin, Paris, France

    Anne Godier

  6. Laboratoire des Biomolécules et de l’Environnement EA 4215, Centre de phytopharmacie, 58 avenue P. Alduy, 66860, Perpignan, France

    Nicolas Inguimbert

  7. Service d’hématologie biologique, AP-HP, Hôpital Ambroise Pare, Boulogne-Billancourt, France

    Delphine Borgel

  8. Faculté de Pharmacie, Université Paris XI, Chatenay Malabry, France

    Delphine Borgel

  9. INSERM UMR 745, UFR des Sciences Pharmaceutiques et Biologiques, Paris, France

    Ivan Bièche

  10. Laboratory of Angiogenesis and Neurovascular Link, Department of Oncology, Vesalius Research Center, University of Leuven, Leuven, Belgium

    Carmen Roncal & Peter Carmeliet

  11. Laboratory of Angiogenesis and Neurovascular Link, Vesalius Research Center, VIB, Leuven, Belgium

    Carmen Roncal & Peter Carmeliet

  12. UF Pharmacocinétique et Pharmacochimie, AP-HP, Hôpital Cochin, Paris, France

    Michel Vidal

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  1. Clément d’Audigier
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  2. Benoit Gautier
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  16. Carmen Roncal
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  18. Michel Vidal
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  19. Pascale Gaussem
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  20. David M. Smadja
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Corresponding author

Correspondence to David M. Smadja.

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d’Audigier, C., Gautier, B., Yon, A. et al. Targeting VEGFR1 on endothelial progenitors modulates their differentiation potential. Angiogenesis 17, 603–616 (2014). https://doi.org/10.1007/s10456-013-9413-2

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