TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability

Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2), are known signaling molecules that increase endothelial barrier permeability. In this study, we investigated the roles of redox-sensitive transient receptor potential (TRP) ion channels, TRPM2, TRPV2 and TRPV4, in H2O2-induced endothel...

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Main Authors: Lena Schaller, Martina Kiefmann, Thomas Gudermann, Alexander Dietrich
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231725002332
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author Lena Schaller
Martina Kiefmann
Thomas Gudermann
Alexander Dietrich
author_facet Lena Schaller
Martina Kiefmann
Thomas Gudermann
Alexander Dietrich
author_sort Lena Schaller
collection DOAJ
description Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2), are known signaling molecules that increase endothelial barrier permeability. In this study, we investigated the roles of redox-sensitive transient receptor potential (TRP) ion channels, TRPM2, TRPV2 and TRPV4, in H2O2-induced endothelial barrier dysfunction. Using primary human pulmonary microvascular endothelial cells (HPMEC), we employed impedance-based resistance measurements, Western blot, and immunofluorescence staining to assess the effects of H2O2 on the endothelial barrier. Exposure to sublytic concentrations of H2O2 caused an acute loss of endothelial barrier integrity, accompanied by the cleavage of vascular endothelial cadherin (VE-cadherin), which was also apparent after application of the TRPV2 activator cannabidiol. The inhibition of either TRPV2 with tranilast or a disintegrin and metalloprotease domain-containing protein 10 (ADAM10) with GI254023X significantly reduced H2O2-induced VE-cadherin cleavage, while TRPM2 inhibition by econazole significantly increased H2O2-driven VE-cadherin cleavage and blockage of TRPV4 showed no effect. Although inhibition of either TRPV2 or ADAM10 did not prevent the initial loss of barrier resistance upon H2O2 exposure, both were essential for the subsequent recovery of barrier integrity. Time-course immunofluorescence stainings revealed that HPMEC barrier recovery involved a transient localization of N-cadherin proteins at adherens junctions. This process of cadherin-switching did not occur upon inhibition of TRPV2 or ADAM10. Our results highlight a novel role for TRPV2 as a redox sensitive ion channels in the microvascular endothelium and provide insight into the mechanisms underlying pulmonary microvascular endothelial barrier recovery.
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spelling doaj-art-7f4e26a3a4e840ba90d48ca9dfd606692025-08-24T05:12:18ZengElsevierRedox Biology2213-23172025-09-018510372010.1016/j.redox.2025.103720TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeabilityLena Schaller0Martina Kiefmann1Thomas Gudermann2Alexander Dietrich3Walther Straub Institute of Pharmacology and Toxicology, Member of the German Center for Lung Research (DZL), Medical Faculty, LMU Munich, Nußbaumstrasse 26, 80336, Munich, GermanyWalther Straub Institute of Pharmacology and Toxicology, Member of the German Center for Lung Research (DZL), Medical Faculty, LMU Munich, Nußbaumstrasse 26, 80336, Munich, GermanyWalther Straub Institute of Pharmacology and Toxicology, Member of the German Center for Lung Research (DZL), Medical Faculty, LMU Munich, Nußbaumstrasse 26, 80336, Munich, GermanyCorresponding author.; Walther Straub Institute of Pharmacology and Toxicology, Member of the German Center for Lung Research (DZL), Medical Faculty, LMU Munich, Nußbaumstrasse 26, 80336, Munich, GermanyReactive oxygen species (ROS), such as hydrogen peroxide (H2O2), are known signaling molecules that increase endothelial barrier permeability. In this study, we investigated the roles of redox-sensitive transient receptor potential (TRP) ion channels, TRPM2, TRPV2 and TRPV4, in H2O2-induced endothelial barrier dysfunction. Using primary human pulmonary microvascular endothelial cells (HPMEC), we employed impedance-based resistance measurements, Western blot, and immunofluorescence staining to assess the effects of H2O2 on the endothelial barrier. Exposure to sublytic concentrations of H2O2 caused an acute loss of endothelial barrier integrity, accompanied by the cleavage of vascular endothelial cadherin (VE-cadherin), which was also apparent after application of the TRPV2 activator cannabidiol. The inhibition of either TRPV2 with tranilast or a disintegrin and metalloprotease domain-containing protein 10 (ADAM10) with GI254023X significantly reduced H2O2-induced VE-cadherin cleavage, while TRPM2 inhibition by econazole significantly increased H2O2-driven VE-cadherin cleavage and blockage of TRPV4 showed no effect. Although inhibition of either TRPV2 or ADAM10 did not prevent the initial loss of barrier resistance upon H2O2 exposure, both were essential for the subsequent recovery of barrier integrity. Time-course immunofluorescence stainings revealed that HPMEC barrier recovery involved a transient localization of N-cadherin proteins at adherens junctions. This process of cadherin-switching did not occur upon inhibition of TRPV2 or ADAM10. Our results highlight a novel role for TRPV2 as a redox sensitive ion channels in the microvascular endothelium and provide insight into the mechanisms underlying pulmonary microvascular endothelial barrier recovery.http://www.sciencedirect.com/science/article/pii/S2213231725002332TRPV2ADAM10ROSImpedanceCadherinEndothelial barrier function
spellingShingle Lena Schaller
Martina Kiefmann
Thomas Gudermann
Alexander Dietrich
TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
Redox Biology
TRPV2
ADAM10
ROS
Impedance
Cadherin
Endothelial barrier function
title TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
title_full TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
title_fullStr TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
title_full_unstemmed TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
title_short TRPV2 channels facilitate pulmonary endothelial barrier recovery after ROS-induced permeability
title_sort trpv2 channels facilitate pulmonary endothelial barrier recovery after ros induced permeability
topic TRPV2
ADAM10
ROS
Impedance
Cadherin
Endothelial barrier function
url http://www.sciencedirect.com/science/article/pii/S2213231725002332
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AT martinakiefmann trpv2channelsfacilitatepulmonaryendothelialbarrierrecoveryafterrosinducedpermeability
AT thomasgudermann trpv2channelsfacilitatepulmonaryendothelialbarrierrecoveryafterrosinducedpermeability
AT alexanderdietrich trpv2channelsfacilitatepulmonaryendothelialbarrierrecoveryafterrosinducedpermeability