The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo

Abigail Woodfin; Mathieu-Benoit Voisin; Martina Beyrau; Bartomeu Colom; Dorothée Caille; Frantzeska-Maria Diapouli; Gerard B Nash; Triantafyllos Chavakis; Steven M Albelda; G Ed Rainger; Paolo Meda; Beat A Imhof; Sussan Nourshargh

doi:10.1038/ni.2062

The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo

Abigail Woodfin, Mathieu-Benoit Voisin, Martina Beyrau, Bartomeu Colom, Dorothée Caille, Frantzeska-Maria Diapouli, Gerard B Nash, Triantafyllos Chavakis, Steven M Albelda, G Ed Rainger, Paolo Meda, Beat A Imhof, Sussan Nourshargh

Cardiovascular Sciences

Research output: Contribution to journal › Article › peer-review

353 Citations (Scopus)

Abstract

The migration of neutrophils into inflamed tissues is a fundamental component of innate immunity. A decisive step in this process is the polarized migration of blood neutrophils through endothelial cells (ECs) lining the venular lumen (transendothelial migration (TEM)) in a luminal-to-abluminal direction. By real-time confocal imaging, we found that neutrophils had disrupted polarized TEM ('hesitant' and 'reverse') in vivo. We noted these events in inflammation after ischemia-reperfusion injury, characterized by lower expression of junctional adhesion molecule C (JAM-C) at EC junctions, and they were enhanced by blockade or genetic deletion of JAM-C in ECs. Our results identify JAM-C as a key regulator of polarized neutrophil TEM in vivo and suggest that reverse TEM of neutrophils can contribute to the dissemination of systemic inflammation.

Original language	English
Pages (from-to)	761-9
Number of pages	9
Journal	Nature Immunology
Volume	12
Issue number	8
DOIs	https://doi.org/10.1038/ni.2062
Publication status	Published - Aug 2011

Keywords

Microscopy, Confocal
Animals
Neutrophils
Mice
Transendothelial and Transepithelial Migration
Image Processing, Computer-Assisted
Cell Adhesion Molecules
Endothelium, Vascular
Reperfusion Injury
Inflammation
Immunoglobulins

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title = "The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo",

abstract = "The migration of neutrophils into inflamed tissues is a fundamental component of innate immunity. A decisive step in this process is the polarized migration of blood neutrophils through endothelial cells (ECs) lining the venular lumen (transendothelial migration (TEM)) in a luminal-to-abluminal direction. By real-time confocal imaging, we found that neutrophils had disrupted polarized TEM ('hesitant' and 'reverse') in vivo. We noted these events in inflammation after ischemia-reperfusion injury, characterized by lower expression of junctional adhesion molecule C (JAM-C) at EC junctions, and they were enhanced by blockade or genetic deletion of JAM-C in ECs. Our results identify JAM-C as a key regulator of polarized neutrophil TEM in vivo and suggest that reverse TEM of neutrophils can contribute to the dissemination of systemic inflammation.",

keywords = "Microscopy, Confocal, Animals, Neutrophils, Mice, Transendothelial and Transepithelial Migration, Image Processing, Computer-Assisted, Cell Adhesion Molecules, Endothelium, Vascular, Reperfusion Injury, Inflammation, Immunoglobulins",

author = "Abigail Woodfin and Mathieu-Benoit Voisin and Martina Beyrau and Bartomeu Colom and Doroth{\'e}e Caille and Frantzeska-Maria Diapouli and Nash, {Gerard B} and Triantafyllos Chavakis and Albelda, {Steven M} and Rainger, {G Ed} and Paolo Meda and Imhof, {Beat A} and Sussan Nourshargh",

year = "2011",

month = aug,

doi = "10.1038/ni.2062",

language = "English",

volume = "12",

pages = "761--9",

journal = "Nature Immunology",

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T1 - The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo

AU - Woodfin, Abigail

AU - Voisin, Mathieu-Benoit

AU - Beyrau, Martina

AU - Colom, Bartomeu

AU - Caille, Dorothée

AU - Diapouli, Frantzeska-Maria

AU - Nash, Gerard B

AU - Chavakis, Triantafyllos

AU - Albelda, Steven M

AU - Rainger, G Ed

AU - Meda, Paolo

AU - Imhof, Beat A

AU - Nourshargh, Sussan

PY - 2011/8

Y1 - 2011/8

N2 - The migration of neutrophils into inflamed tissues is a fundamental component of innate immunity. A decisive step in this process is the polarized migration of blood neutrophils through endothelial cells (ECs) lining the venular lumen (transendothelial migration (TEM)) in a luminal-to-abluminal direction. By real-time confocal imaging, we found that neutrophils had disrupted polarized TEM ('hesitant' and 'reverse') in vivo. We noted these events in inflammation after ischemia-reperfusion injury, characterized by lower expression of junctional adhesion molecule C (JAM-C) at EC junctions, and they were enhanced by blockade or genetic deletion of JAM-C in ECs. Our results identify JAM-C as a key regulator of polarized neutrophil TEM in vivo and suggest that reverse TEM of neutrophils can contribute to the dissemination of systemic inflammation.

AB - The migration of neutrophils into inflamed tissues is a fundamental component of innate immunity. A decisive step in this process is the polarized migration of blood neutrophils through endothelial cells (ECs) lining the venular lumen (transendothelial migration (TEM)) in a luminal-to-abluminal direction. By real-time confocal imaging, we found that neutrophils had disrupted polarized TEM ('hesitant' and 'reverse') in vivo. We noted these events in inflammation after ischemia-reperfusion injury, characterized by lower expression of junctional adhesion molecule C (JAM-C) at EC junctions, and they were enhanced by blockade or genetic deletion of JAM-C in ECs. Our results identify JAM-C as a key regulator of polarized neutrophil TEM in vivo and suggest that reverse TEM of neutrophils can contribute to the dissemination of systemic inflammation.

KW - Microscopy, Confocal

KW - Animals

KW - Neutrophils

KW - Mice

KW - Transendothelial and Transepithelial Migration

KW - Image Processing, Computer-Assisted

KW - Cell Adhesion Molecules

KW - Endothelium, Vascular

KW - Reperfusion Injury

KW - Inflammation

KW - Immunoglobulins

U2 - 10.1038/ni.2062

DO - 10.1038/ni.2062

M3 - Article

C2 - 21706006

SN - 1529-2916

VL - 12

SP - 761

EP - 769

JO - Nature Immunology

JF - Nature Immunology

IS - 8

ER -

The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo

Abstract

Keywords

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