Cargando…

The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation

Leukocyte transendothelial migration involves the active participation of the endothelium through the formation of apical membrane protrusions that embrace adherent leukocytes, termed docking structures. Using live-cell imaging, we find that prior to transmigration, endothelial docking structures fo...

Descripción completa

Detalles Bibliográficos
Autores principales: van Rijssel, Jos, Kroon, Jeffrey, Hoogenboezem, Mark, van Alphen, Floris P. J., de Jong, Renske J., Kostadinova, Elena, Geerts, Dirk, Hordijk, Peter L., van Buul, Jaap D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3408411/
https://www.ncbi.nlm.nih.gov/pubmed/22696684
http://dx.doi.org/10.1091/mbc.E11-11-0907
_version_ 1782239454629462016
author van Rijssel, Jos
Kroon, Jeffrey
Hoogenboezem, Mark
van Alphen, Floris P. J.
de Jong, Renske J.
Kostadinova, Elena
Geerts, Dirk
Hordijk, Peter L.
van Buul, Jaap D.
author_facet van Rijssel, Jos
Kroon, Jeffrey
Hoogenboezem, Mark
van Alphen, Floris P. J.
de Jong, Renske J.
Kostadinova, Elena
Geerts, Dirk
Hordijk, Peter L.
van Buul, Jaap D.
author_sort van Rijssel, Jos
collection PubMed
description Leukocyte transendothelial migration involves the active participation of the endothelium through the formation of apical membrane protrusions that embrace adherent leukocytes, termed docking structures. Using live-cell imaging, we find that prior to transmigration, endothelial docking structures form around 80% of all neutrophils. Previously we showed that endothelial RhoG and SGEF control leukocyte transmigration. In this study, our data reveal that both full-length Trio and the first DH-PH (TrioD1) domain of Trio, which can activate Rac1 and RhoG, interact with ICAM-1 and are recruited to leukocyte adhesion sites. Moreover, upon clustering of ICAM-1, the Rho-guanine nucleotide exchange factor Trio activates Rac1, prior to activating RhoG, in a filamin-dependent manner. We further show that docking structure formation is initiated by ICAM-1 clustering into ring-like structures, which is followed by apical membrane protrusion. Interestingly, we find that Rac1 is required for ICAM-1 clustering, whereas RhoG controls membrane protrusion formation. Finally, silencing endothelial Trio expression or reducing TrioD1 activity without affecting SGEF impairs both docking structure formation and leukocyte transmigration. We conclude that Trio promotes leukocyte transendothelial migration by inducing endothelial docking structure formation in a filamin-dependent manner through the activation of Rac1 and RhoG.
format Online
Article
Text
id pubmed-3408411
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher The American Society for Cell Biology
record_format MEDLINE/PubMed
spelling pubmed-34084112012-10-16 The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation van Rijssel, Jos Kroon, Jeffrey Hoogenboezem, Mark van Alphen, Floris P. J. de Jong, Renske J. Kostadinova, Elena Geerts, Dirk Hordijk, Peter L. van Buul, Jaap D. Mol Biol Cell Articles Leukocyte transendothelial migration involves the active participation of the endothelium through the formation of apical membrane protrusions that embrace adherent leukocytes, termed docking structures. Using live-cell imaging, we find that prior to transmigration, endothelial docking structures form around 80% of all neutrophils. Previously we showed that endothelial RhoG and SGEF control leukocyte transmigration. In this study, our data reveal that both full-length Trio and the first DH-PH (TrioD1) domain of Trio, which can activate Rac1 and RhoG, interact with ICAM-1 and are recruited to leukocyte adhesion sites. Moreover, upon clustering of ICAM-1, the Rho-guanine nucleotide exchange factor Trio activates Rac1, prior to activating RhoG, in a filamin-dependent manner. We further show that docking structure formation is initiated by ICAM-1 clustering into ring-like structures, which is followed by apical membrane protrusion. Interestingly, we find that Rac1 is required for ICAM-1 clustering, whereas RhoG controls membrane protrusion formation. Finally, silencing endothelial Trio expression or reducing TrioD1 activity without affecting SGEF impairs both docking structure formation and leukocyte transmigration. We conclude that Trio promotes leukocyte transendothelial migration by inducing endothelial docking structure formation in a filamin-dependent manner through the activation of Rac1 and RhoG. The American Society for Cell Biology 2012-08-01 /pmc/articles/PMC3408411/ /pubmed/22696684 http://dx.doi.org/10.1091/mbc.E11-11-0907 Text en © 2012 van Rijssel et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell BD; are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
van Rijssel, Jos
Kroon, Jeffrey
Hoogenboezem, Mark
van Alphen, Floris P. J.
de Jong, Renske J.
Kostadinova, Elena
Geerts, Dirk
Hordijk, Peter L.
van Buul, Jaap D.
The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title_full The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title_fullStr The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title_full_unstemmed The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title_short The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation
title_sort rho-guanine nucleotide exchange factor trio controls leukocyte transendothelial migration by promoting docking structure formation
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3408411/
https://www.ncbi.nlm.nih.gov/pubmed/22696684
http://dx.doi.org/10.1091/mbc.E11-11-0907
work_keys_str_mv AT vanrijsseljos therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT kroonjeffrey therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT hoogenboezemmark therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT vanalphenflorispj therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT dejongrenskej therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT kostadinovaelena therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT geertsdirk therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT hordijkpeterl therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT vanbuuljaapd therhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT vanrijsseljos rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT kroonjeffrey rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT hoogenboezemmark rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT vanalphenflorispj rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT dejongrenskej rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT kostadinovaelena rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT geertsdirk rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT hordijkpeterl rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation
AT vanbuuljaapd rhoguaninenucleotideexchangefactortriocontrolsleukocytetransendothelialmigrationbypromotingdockingstructureformation