Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia

Abstract Increased levels of soluble endoglin (sEng) are found in serum, plasma, and urine of preeclampsia patients. sEng is released from membrane-bound endoglin through the proteolytic activity of metalloproteases, but its structural heterogeneity suggests the involvement of additional proteases....

Full description

Saved in:
Bibliographic Details
Main Authors: Divina El Hamaoui, Aurore Marchelli, Sophie Gandrille, Etienne Reboul, Alain Stepanian, Bruno Palmier, Luca Jovine, Franck Lebrin, David M. Smadja, Carmelo Bernabeu, Cecile V. Denis, Pascale Gaussem, Samuela Pasquali, Alexandre Kauskot, Elisa Rossi
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07751-3
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850029126828687360
author Divina El Hamaoui
Aurore Marchelli
Sophie Gandrille
Etienne Reboul
Alain Stepanian
Bruno Palmier
Luca Jovine
Franck Lebrin
David M. Smadja
Carmelo Bernabeu
Cecile V. Denis
Pascale Gaussem
Samuela Pasquali
Alexandre Kauskot
Elisa Rossi
author_facet Divina El Hamaoui
Aurore Marchelli
Sophie Gandrille
Etienne Reboul
Alain Stepanian
Bruno Palmier
Luca Jovine
Franck Lebrin
David M. Smadja
Carmelo Bernabeu
Cecile V. Denis
Pascale Gaussem
Samuela Pasquali
Alexandre Kauskot
Elisa Rossi
author_sort Divina El Hamaoui
collection DOAJ
description Abstract Increased levels of soluble endoglin (sEng) are found in serum, plasma, and urine of preeclampsia patients. sEng is released from membrane-bound endoglin through the proteolytic activity of metalloproteases, but its structural heterogeneity suggests the involvement of additional proteases. Considering the roles of thrombin and sEng in preeclampsia pathogenesis, we investigated whether thrombin cleaves endoglin. Sequence analysis revealed a conserved peptide in endoglin similar to the α-thrombin cleavage site of protease-activated receptor-1. Western blot analysis of plasma from preeclamptic women showed endoglin fragments consistent with thrombin-mediated cleavage. Incubation of purified endoglin with thrombin generated specific fragments, whose N- and C-terminal sequencing confirmed the predicted cleavage sites. Furthermore, thrombin treatment of endoglin-expressing cells released sEng and reduced cell surface endoglin. These findings suggest that multiple protease-targeted cleavage sites lead to the generation of sEng fragments, which may reflect endothelial dysfunction and preeclampsia progression.
format Article
id doaj-art-1cbb7d4d40fe4d78ba3fc1abc02cb0e5
institution DOAJ
issn 2399-3642
language English
publishDate 2025-02-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-1cbb7d4d40fe4d78ba3fc1abc02cb0e52025-08-20T02:59:37ZengNature PortfolioCommunications Biology2399-36422025-02-018111210.1038/s42003-025-07751-3Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsiaDivina El Hamaoui0Aurore Marchelli1Sophie Gandrille2Etienne Reboul3Alain Stepanian4Bruno Palmier5Luca Jovine6Franck Lebrin7David M. Smadja8Carmelo Bernabeu9Cecile V. Denis10Pascale Gaussem11Samuela Pasquali12Alexandre Kauskot13Elisa Rossi14Innovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéService d’Hématologie biologiqueInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéKarolinska Institutet, Department of Medicine (MedH)Einthoven Laboratory for Experimental Vascular Medicine, Department of Internal Medicine (Nephrology), Leiden University Medical CenterInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéCentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC)HITh, Unite Mixte de Recherche 1176 INSERM, Université Paris-SaclayInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéLaboratoire Biologie Fonctionnelle et Adaptative, INSERM ERL1133 F-75013HITh, Unite Mixte de Recherche 1176 INSERM, Université Paris-SaclayInnovative Therapies in Hemostasis, INSERM U1140, Université Paris CitéAbstract Increased levels of soluble endoglin (sEng) are found in serum, plasma, and urine of preeclampsia patients. sEng is released from membrane-bound endoglin through the proteolytic activity of metalloproteases, but its structural heterogeneity suggests the involvement of additional proteases. Considering the roles of thrombin and sEng in preeclampsia pathogenesis, we investigated whether thrombin cleaves endoglin. Sequence analysis revealed a conserved peptide in endoglin similar to the α-thrombin cleavage site of protease-activated receptor-1. Western blot analysis of plasma from preeclamptic women showed endoglin fragments consistent with thrombin-mediated cleavage. Incubation of purified endoglin with thrombin generated specific fragments, whose N- and C-terminal sequencing confirmed the predicted cleavage sites. Furthermore, thrombin treatment of endoglin-expressing cells released sEng and reduced cell surface endoglin. These findings suggest that multiple protease-targeted cleavage sites lead to the generation of sEng fragments, which may reflect endothelial dysfunction and preeclampsia progression.https://doi.org/10.1038/s42003-025-07751-3
spellingShingle Divina El Hamaoui
Aurore Marchelli
Sophie Gandrille
Etienne Reboul
Alain Stepanian
Bruno Palmier
Luca Jovine
Franck Lebrin
David M. Smadja
Carmelo Bernabeu
Cecile V. Denis
Pascale Gaussem
Samuela Pasquali
Alexandre Kauskot
Elisa Rossi
Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
Communications Biology
title Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
title_full Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
title_fullStr Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
title_full_unstemmed Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
title_short Thrombin cleaves membrane-bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
title_sort thrombin cleaves membrane bound endoglin potentially contributing to the heterogeneity of circulating endoglin in preeclampsia
url https://doi.org/10.1038/s42003-025-07751-3
work_keys_str_mv AT divinaelhamaoui thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT auroremarchelli thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT sophiegandrille thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT etiennereboul thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT alainstepanian thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT brunopalmier thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT lucajovine thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT francklebrin thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT davidmsmadja thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT carmelobernabeu thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT cecilevdenis thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT pascalegaussem thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT samuelapasquali thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT alexandrekauskot thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia
AT elisarossi thrombincleavesmembraneboundendoglinpotentiallycontributingtotheheterogeneityofcirculatingendoglininpreeclampsia