IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability

Abstract Background Hemorrhagic shock (HS) corresponds to absolute hypovolemia creating an imbalance between oxygen supply and consumption. This causes an impaired hemostasis, a systemic inflammatory response, and microvascular permeability which can lead to multiple organ failure (MOF). There is no...

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Main Authors: Nathalie Baudry, Aurélie Campeanu, Clotilde Aussel, Caroline Doutrelon, Marion Grosbot, Sébastien Banzet, Eric Vicaut, Juliette Peltzer
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-024-05961-7
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author Nathalie Baudry
Aurélie Campeanu
Clotilde Aussel
Caroline Doutrelon
Marion Grosbot
Sébastien Banzet
Eric Vicaut
Juliette Peltzer
author_facet Nathalie Baudry
Aurélie Campeanu
Clotilde Aussel
Caroline Doutrelon
Marion Grosbot
Sébastien Banzet
Eric Vicaut
Juliette Peltzer
author_sort Nathalie Baudry
collection DOAJ
description Abstract Background Hemorrhagic shock (HS) corresponds to absolute hypovolemia creating an imbalance between oxygen supply and consumption. This causes an impaired hemostasis, a systemic inflammatory response, and microvascular permeability which can lead to multiple organ failure (MOF). There is no specific treatment for the endothelial dysfunction that plays a major role in the evolution towards MOF. Mesenchymal stromal cells (MSC) have been used in clinical trials for their immunomodulation and tissue repair capabilities for many years. Moreover, we previously showed that IL-1β-primed-MSC (MSCp) attenuated HS-induced organ injuries. The objective of the study was to determine whether MSCp could prevent the onset of MOF after HS by preventing endothelial dysfunction. Methods We established a rat model of HS, inducing 90 min of HS at a fixed mean arterial pressure of 35 mmHg, followed by resuscitation and transfusion. MSCp treatment was administered intravenously at the onset of resuscitation. After 6 h, we assessed plasma levels of endothelial markers, vascular permeability using Evans Blue (EB) dye, and renal and hepatic water content by measuring the wet-to-dry weight difference. Additionally, we investigated the ability of MSCp to inhibit leukocyte adhesion to activated endothelium in vitro. Results Our results indicate that early administration of MSCp significantly reduced the percentage of water content and EB dye in the liver but not in the kidney. These results were associated with a trend toward decreased plasma levels of Syndecan-1, ICAM-1, vWF, and VCAM-1. In vitro, MSCp reduced leukocyte-endothelial cell adhesion. Together, our results suggest that MSCp help to prevent endothelial dysfunction and vascular leakage, which, in turn, could protect the liver from injury.
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spelling doaj-art-d0fe8fe78c564dc29812dc802f72f15d2025-08-20T02:39:37ZengBMCJournal of Translational Medicine1479-58762024-12-0122111210.1186/s12967-024-05961-7IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeabilityNathalie Baudry0Aurélie Campeanu1Clotilde Aussel2Caroline Doutrelon3Marion Grosbot4Sébastien Banzet5Eric Vicaut6Juliette Peltzer7Laboratoire d’Etude de La Microcirculation, UMRS 942 INSERM, Université Paris CitéLaboratoire d’Etude de La Microcirculation, UMRS 942 INSERM, Université Paris CitéInstitut de Recherche Biomédicale Des Armées (IRBA)Institut de Recherche Biomédicale Des Armées (IRBA)Institut de Recherche Biomédicale Des Armées (IRBA)Institut de Recherche Biomédicale Des Armées (IRBA)Laboratoire d’Etude de La Microcirculation, UMRS 942 INSERM, Université Paris CitéInstitut de Recherche Biomédicale Des Armées (IRBA)Abstract Background Hemorrhagic shock (HS) corresponds to absolute hypovolemia creating an imbalance between oxygen supply and consumption. This causes an impaired hemostasis, a systemic inflammatory response, and microvascular permeability which can lead to multiple organ failure (MOF). There is no specific treatment for the endothelial dysfunction that plays a major role in the evolution towards MOF. Mesenchymal stromal cells (MSC) have been used in clinical trials for their immunomodulation and tissue repair capabilities for many years. Moreover, we previously showed that IL-1β-primed-MSC (MSCp) attenuated HS-induced organ injuries. The objective of the study was to determine whether MSCp could prevent the onset of MOF after HS by preventing endothelial dysfunction. Methods We established a rat model of HS, inducing 90 min of HS at a fixed mean arterial pressure of 35 mmHg, followed by resuscitation and transfusion. MSCp treatment was administered intravenously at the onset of resuscitation. After 6 h, we assessed plasma levels of endothelial markers, vascular permeability using Evans Blue (EB) dye, and renal and hepatic water content by measuring the wet-to-dry weight difference. Additionally, we investigated the ability of MSCp to inhibit leukocyte adhesion to activated endothelium in vitro. Results Our results indicate that early administration of MSCp significantly reduced the percentage of water content and EB dye in the liver but not in the kidney. These results were associated with a trend toward decreased plasma levels of Syndecan-1, ICAM-1, vWF, and VCAM-1. In vitro, MSCp reduced leukocyte-endothelial cell adhesion. Together, our results suggest that MSCp help to prevent endothelial dysfunction and vascular leakage, which, in turn, could protect the liver from injury.https://doi.org/10.1186/s12967-024-05961-7Mesenchymal stromal cellsPriming IL-1βHemorrhagic shockVascular permeabilityMultiple organ failure
spellingShingle Nathalie Baudry
Aurélie Campeanu
Clotilde Aussel
Caroline Doutrelon
Marion Grosbot
Sébastien Banzet
Eric Vicaut
Juliette Peltzer
IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
Journal of Translational Medicine
Mesenchymal stromal cells
Priming IL-1β
Hemorrhagic shock
Vascular permeability
Multiple organ failure
title IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
title_full IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
title_fullStr IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
title_full_unstemmed IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
title_short IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced vascular permeability
title_sort il 1β primed mesenchymal stromal cells moderate hemorrhagic shock induced vascular permeability
topic Mesenchymal stromal cells
Priming IL-1β
Hemorrhagic shock
Vascular permeability
Multiple organ failure
url https://doi.org/10.1186/s12967-024-05961-7
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