Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly

Development and homeostasis of blood vessels critically depend on the regulation of endothelial cell–cell junctions. VE-cadherin (VEcad)-based cell–cell junctions are connected to the actin cytoskeleton and regulated by actin-binding proteins. Coronin 1B (Coro1B) is an actin binding protein that con...

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Main Authors: Ann-Cathrin Werner, Ludwig T. Weckbach, Melanie Salvermoser, Bettina Pitter, Jiahui Cao, Daniela Maier-Begandt, Ignasi Forné, Hans-Joachim Schnittler, Barbara Walzog, Eloi Montanez
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcell.2020.00708/full
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author Ann-Cathrin Werner
Ann-Cathrin Werner
Ludwig T. Weckbach
Ludwig T. Weckbach
Ludwig T. Weckbach
Melanie Salvermoser
Melanie Salvermoser
Bettina Pitter
Bettina Pitter
Jiahui Cao
Daniela Maier-Begandt
Daniela Maier-Begandt
Ignasi Forné
Hans-Joachim Schnittler
Barbara Walzog
Barbara Walzog
Eloi Montanez
Eloi Montanez
Eloi Montanez
author_facet Ann-Cathrin Werner
Ann-Cathrin Werner
Ludwig T. Weckbach
Ludwig T. Weckbach
Ludwig T. Weckbach
Melanie Salvermoser
Melanie Salvermoser
Bettina Pitter
Bettina Pitter
Jiahui Cao
Daniela Maier-Begandt
Daniela Maier-Begandt
Ignasi Forné
Hans-Joachim Schnittler
Barbara Walzog
Barbara Walzog
Eloi Montanez
Eloi Montanez
Eloi Montanez
author_sort Ann-Cathrin Werner
collection DOAJ
description Development and homeostasis of blood vessels critically depend on the regulation of endothelial cell–cell junctions. VE-cadherin (VEcad)-based cell–cell junctions are connected to the actin cytoskeleton and regulated by actin-binding proteins. Coronin 1B (Coro1B) is an actin binding protein that controls actin networks at classical lamellipodia. The role of Coro1B in endothelial cells (ECs) is not fully understood and investigated in this study. Here, we demonstrate that Coro1B is a novel component and regulator of cell–cell junctions in ECs. Immunofluorescence studies show that Coro1B colocalizes with VEcad at cell–cell junctions in monolayers of ECs. Live-cell imaging reveals that Coro1B is recruited to, and operated at actin-driven membrane protrusions at cell–cell junctions. Coro1B is recruited to cell–cell junctions via a mechanism that requires the relaxation of the actomyosin cytoskeleton. By analyzing the Coro1B interactome, we identify integrin-linked kinase (ILK) as new Coro1B-associated protein. Coro1B colocalizes with α-parvin, an interactor of ILK, at the leading edge of lamellipodia protrusions. Functional experiments reveal that depletion of Coro1B causes defects in the actin cytoskeleton and cell–cell junctions. Finally, in matrigel tube network assays, depletion of Coro1B results in reduced network complexity, tube number and tube length. Together, our findings point toward a critical role for Coro1B in the dynamic remodeling of endothelial cell–cell junctions and the assembly of endothelial networks.
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spelling doaj.art-bc7e317cdb204177bdc12eef21140c532022-12-22T00:01:48ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-07-01810.3389/fcell.2020.00708568975Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network AssemblyAnn-Cathrin Werner0Ann-Cathrin Werner1Ludwig T. Weckbach2Ludwig T. Weckbach3Ludwig T. Weckbach4Melanie Salvermoser5Melanie Salvermoser6Bettina Pitter7Bettina Pitter8Jiahui Cao9Daniela Maier-Begandt10Daniela Maier-Begandt11Ignasi Forné12Hans-Joachim Schnittler13Barbara Walzog14Barbara Walzog15Eloi Montanez16Eloi Montanez17Eloi Montanez18Institute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyMedizinische Klinik I, Klinikum Großhadern, Munich, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyInstitute of Anatomy and Vascular Biology, Westfälische Wilhelms-Universität Münster, Münster, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyProtein Analysis Unit, Biomedical Center, LMU Munich, Munich, GermanyInstitute of Anatomy and Vascular Biology, Westfälische Wilhelms-Universität Münster, Münster, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyInstitute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, LMU Munich, Munich, GermanyWalter Brendel Center of Experimental Medicine, University Hospital, LMU Munich, Munich, GermanyDepartment of Physiological Sciences, Faculty of Medicine and Health Sciences, University of Barcelona and IDIBELL, Barcelona, SpainDevelopment and homeostasis of blood vessels critically depend on the regulation of endothelial cell–cell junctions. VE-cadherin (VEcad)-based cell–cell junctions are connected to the actin cytoskeleton and regulated by actin-binding proteins. Coronin 1B (Coro1B) is an actin binding protein that controls actin networks at classical lamellipodia. The role of Coro1B in endothelial cells (ECs) is not fully understood and investigated in this study. Here, we demonstrate that Coro1B is a novel component and regulator of cell–cell junctions in ECs. Immunofluorescence studies show that Coro1B colocalizes with VEcad at cell–cell junctions in monolayers of ECs. Live-cell imaging reveals that Coro1B is recruited to, and operated at actin-driven membrane protrusions at cell–cell junctions. Coro1B is recruited to cell–cell junctions via a mechanism that requires the relaxation of the actomyosin cytoskeleton. By analyzing the Coro1B interactome, we identify integrin-linked kinase (ILK) as new Coro1B-associated protein. Coro1B colocalizes with α-parvin, an interactor of ILK, at the leading edge of lamellipodia protrusions. Functional experiments reveal that depletion of Coro1B causes defects in the actin cytoskeleton and cell–cell junctions. Finally, in matrigel tube network assays, depletion of Coro1B results in reduced network complexity, tube number and tube length. Together, our findings point toward a critical role for Coro1B in the dynamic remodeling of endothelial cell–cell junctions and the assembly of endothelial networks.https://www.frontiersin.org/article/10.3389/fcell.2020.00708/fullendothelial cellscell–cell junctionactintube formationcoronin 1B
spellingShingle Ann-Cathrin Werner
Ann-Cathrin Werner
Ludwig T. Weckbach
Ludwig T. Weckbach
Ludwig T. Weckbach
Melanie Salvermoser
Melanie Salvermoser
Bettina Pitter
Bettina Pitter
Jiahui Cao
Daniela Maier-Begandt
Daniela Maier-Begandt
Ignasi Forné
Hans-Joachim Schnittler
Barbara Walzog
Barbara Walzog
Eloi Montanez
Eloi Montanez
Eloi Montanez
Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
Frontiers in Cell and Developmental Biology
endothelial cells
cell–cell junction
actin
tube formation
coronin 1B
title Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
title_full Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
title_fullStr Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
title_full_unstemmed Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
title_short Coronin 1B Controls Endothelial Actin Dynamics at Cell–Cell Junctions and Is Required for Endothelial Network Assembly
title_sort coronin 1b controls endothelial actin dynamics at cell cell junctions and is required for endothelial network assembly
topic endothelial cells
cell–cell junction
actin
tube formation
coronin 1B
url https://www.frontiersin.org/article/10.3389/fcell.2020.00708/full
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