Thrombin receptor PAR1 silencing in endothelial colony-forming cells modifies stemness and vasculogenic properties.


Journal

Journal of thrombosis and haemostasis : JTH
ISSN: 1538-7836
Titre abrégé: J Thromb Haemost
Pays: England
ID NLM: 101170508

Informations de publication

Date de publication:
12 2023
Historique:
received: 03 07 2023
revised: 09 08 2023
accepted: 28 08 2023
medline: 27 11 2023
pubmed: 8 9 2023
entrez: 7 9 2023
Statut: ppublish

Résumé

The involvement of thrombin receptor PAR1 in blood vessel development has been largely demonstrated in knockout mice; however, its implication in adult mouse angiogenesis seems very moderate. We aimed to explore the potential relationships between PAR1, stemness, and angiogenic properties of human endothelial colony-forming cells (ECFCs). PAR1 activation on ECFCs using the selective PAR1-activating peptide induced a significant decrease in CD133 expression (RTQ-PCR analysis). In line, silencing of PAR1 gene expression with siRNA increased CD133 mRNA as well as intracellular CD133 protein expression. To confirm the link between CD133 and PAR1, we explored the association between PAR1 and CD133 levels in fast and slow fibroblasts prone to reprogramming. An imbalance between PAR1 and CD133 levels was evidenced, with a decreased expression of PAR1 in fast reprogramming fibroblasts expressing a high CD133 level. Regarding in vitro ECFC angiogenic properties, PAR1 silencing with specific siRNA induced cell proliferation evidenced by the overexpression of Ki67. However, it did not impact migration properties nor ECFC adhesion on smooth muscle cells or human arterial endothelial cells. In a mouse model of hind-limb ischemia, PAR1 silencing in ECFCs significantly increased postischemic revascularization compared to siCtrl-ECFCs along with a significant increase in cutaneous blood flows (P < .0001), microvessel density (P = .02), myofiber regeneration (P < .0001), and human endothelial cell incorporation in muscle (P < .0001). In conclusion, our work describes for the first time a link between PAR1, stemness, and vasculogenesis in human ECFCs.

Sections du résumé

BACKGROUND
The involvement of thrombin receptor PAR1 in blood vessel development has been largely demonstrated in knockout mice; however, its implication in adult mouse angiogenesis seems very moderate.
OBJECTIVES
We aimed to explore the potential relationships between PAR1, stemness, and angiogenic properties of human endothelial colony-forming cells (ECFCs).
METHODS AND RESULTS
PAR1 activation on ECFCs using the selective PAR1-activating peptide induced a significant decrease in CD133 expression (RTQ-PCR analysis). In line, silencing of PAR1 gene expression with siRNA increased CD133 mRNA as well as intracellular CD133 protein expression. To confirm the link between CD133 and PAR1, we explored the association between PAR1 and CD133 levels in fast and slow fibroblasts prone to reprogramming. An imbalance between PAR1 and CD133 levels was evidenced, with a decreased expression of PAR1 in fast reprogramming fibroblasts expressing a high CD133 level. Regarding in vitro ECFC angiogenic properties, PAR1 silencing with specific siRNA induced cell proliferation evidenced by the overexpression of Ki67. However, it did not impact migration properties nor ECFC adhesion on smooth muscle cells or human arterial endothelial cells. In a mouse model of hind-limb ischemia, PAR1 silencing in ECFCs significantly increased postischemic revascularization compared to siCtrl-ECFCs along with a significant increase in cutaneous blood flows (P < .0001), microvessel density (P = .02), myofiber regeneration (P < .0001), and human endothelial cell incorporation in muscle (P < .0001).
CONCLUSION
In conclusion, our work describes for the first time a link between PAR1, stemness, and vasculogenesis in human ECFCs.

Identifiants

pubmed: 37678550
pii: S1538-7836(23)00658-X
doi: 10.1016/j.jtha.2023.08.029
pii:
doi:

Substances chimiques

Receptor, PAR-1 0
Receptors, Thrombin 0
RNA, Small Interfering 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3640-3648

Informations de copyright

Copyright © 2023 International Society on Thrombosis and Haemostasis. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interests There are no competing interests to disclose.

Auteurs

David M Smadja (DM)

Hematology Department, AP-HP, Georges Pompidou European Hospital, Paris, France; Université Paris-Cité, INSERM UMR-S 1140, Innovative Therapies in Haemostasis, Paris, France. Electronic address: david.smadja@aphp.fr.

Elisa Rossi (E)

Université Paris-Cité, INSERM UMR-S 1140, Innovative Therapies in Haemostasis, Paris, France.

Skerdi Haviari (S)

Université Paris-Cité, INSERM UMR-S 1137 (IAME), Paris, France; Département Épidémiologie Biostatistiques et Recherche Clinique, AP-HP, Hôpital Bichat, Paris, France.

Ivan Bieche (I)

Institut Curie, Paris, France.

Audrey Cras (A)

Université Paris-Cité, INSERM UMR-S 1140, Innovative Therapies in Haemostasis, Paris, France; Cell Therapy Unit, AP-HP, Saint Louis Hospital, Paris, France.

Pascale Gaussem (P)

Hematology Department, AP-HP, Georges Pompidou European Hospital, Paris, France; Université Paris-Cité, INSERM UMR-S 1140, Innovative Therapies in Haemostasis, Paris, France.

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Classifications MeSH