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A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites

Neutrophils are abundant circulating leukocytes that are rapidly recruited to sites of inflammation in an integrin-dependent fashion. Contrasting with the well-characterized regulation of integrin activation, mechanisms regulating integrin inactivation remain largely obscure. Using mouse neutrophils...

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Autores principales: McCormick, Barry, Craig, Helen E., Chu, Julia Y., Carlin, Leo M., Canel, Marta, Wollweber, Florian, Toivakka, Matilda, Michael, Melina, Astier, Anne L., Norton, Laura, Lilja, Johanna, Felton, Jennifer M., Sasaki, Takehiko, Ivaska, Johanna, Hers, Ingeborg, Dransfield, Ian, Rossi, Adriano G., Vermeren, Sonja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: AAI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6731454/
https://www.ncbi.nlm.nih.gov/pubmed/31427445
http://dx.doi.org/10.4049/jimmunol.1900443
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author McCormick, Barry
Craig, Helen E.
Chu, Julia Y.
Carlin, Leo M.
Canel, Marta
Wollweber, Florian
Toivakka, Matilda
Michael, Melina
Astier, Anne L.
Norton, Laura
Lilja, Johanna
Felton, Jennifer M.
Sasaki, Takehiko
Ivaska, Johanna
Hers, Ingeborg
Dransfield, Ian
Rossi, Adriano G.
Vermeren, Sonja
author_facet McCormick, Barry
Craig, Helen E.
Chu, Julia Y.
Carlin, Leo M.
Canel, Marta
Wollweber, Florian
Toivakka, Matilda
Michael, Melina
Astier, Anne L.
Norton, Laura
Lilja, Johanna
Felton, Jennifer M.
Sasaki, Takehiko
Ivaska, Johanna
Hers, Ingeborg
Dransfield, Ian
Rossi, Adriano G.
Vermeren, Sonja
author_sort McCormick, Barry
collection PubMed
description Neutrophils are abundant circulating leukocytes that are rapidly recruited to sites of inflammation in an integrin-dependent fashion. Contrasting with the well-characterized regulation of integrin activation, mechanisms regulating integrin inactivation remain largely obscure. Using mouse neutrophils, we demonstrate in this study that the GTPase activating protein ARAP3 is a critical regulator of integrin inactivation; experiments with Chinese hamster ovary cells indicate that this is not restricted to neutrophils. Specifically, ARAP3 acts in a negative feedback loop downstream of PI3K to regulate integrin inactivation. Integrin ligand binding drives the activation of PI3K and of its effectors, including ARAP3, by outside-in signaling. ARAP3, in turn, promotes localized integrin inactivation by negative inside-out signaling. This negative feedback loop reduces integrin-mediated PI3K activity, with ARAP3 effectively switching off its own activator, while promoting turnover of substrate adhesions. In vitro, ARAP3-deficient neutrophils display defective PIP3 polarization, adhesion turnover, and transendothelial migration. In vivo, ARAP3-deficient neutrophils are characterized by a neutrophil-autonomous recruitment defect to sites of inflammation.
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spelling pubmed-67314542019-09-12 A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites McCormick, Barry Craig, Helen E. Chu, Julia Y. Carlin, Leo M. Canel, Marta Wollweber, Florian Toivakka, Matilda Michael, Melina Astier, Anne L. Norton, Laura Lilja, Johanna Felton, Jennifer M. Sasaki, Takehiko Ivaska, Johanna Hers, Ingeborg Dransfield, Ian Rossi, Adriano G. Vermeren, Sonja J Immunol Innate Immunity and Inflammation Neutrophils are abundant circulating leukocytes that are rapidly recruited to sites of inflammation in an integrin-dependent fashion. Contrasting with the well-characterized regulation of integrin activation, mechanisms regulating integrin inactivation remain largely obscure. Using mouse neutrophils, we demonstrate in this study that the GTPase activating protein ARAP3 is a critical regulator of integrin inactivation; experiments with Chinese hamster ovary cells indicate that this is not restricted to neutrophils. Specifically, ARAP3 acts in a negative feedback loop downstream of PI3K to regulate integrin inactivation. Integrin ligand binding drives the activation of PI3K and of its effectors, including ARAP3, by outside-in signaling. ARAP3, in turn, promotes localized integrin inactivation by negative inside-out signaling. This negative feedback loop reduces integrin-mediated PI3K activity, with ARAP3 effectively switching off its own activator, while promoting turnover of substrate adhesions. In vitro, ARAP3-deficient neutrophils display defective PIP3 polarization, adhesion turnover, and transendothelial migration. In vivo, ARAP3-deficient neutrophils are characterized by a neutrophil-autonomous recruitment defect to sites of inflammation. AAI 2019-09-15 2019-08-19 /pmc/articles/PMC6731454/ /pubmed/31427445 http://dx.doi.org/10.4049/jimmunol.1900443 Text en Copyright © 2019 The Authors https://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the CC BY 4.0 Unported license.
spellingShingle Innate Immunity and Inflammation
McCormick, Barry
Craig, Helen E.
Chu, Julia Y.
Carlin, Leo M.
Canel, Marta
Wollweber, Florian
Toivakka, Matilda
Michael, Melina
Astier, Anne L.
Norton, Laura
Lilja, Johanna
Felton, Jennifer M.
Sasaki, Takehiko
Ivaska, Johanna
Hers, Ingeborg
Dransfield, Ian
Rossi, Adriano G.
Vermeren, Sonja
A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title_full A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title_fullStr A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title_full_unstemmed A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title_short A Negative Feedback Loop Regulates Integrin Inactivation and Promotes Neutrophil Recruitment to Inflammatory Sites
title_sort negative feedback loop regulates integrin inactivation and promotes neutrophil recruitment to inflammatory sites
topic Innate Immunity and Inflammation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6731454/
https://www.ncbi.nlm.nih.gov/pubmed/31427445
http://dx.doi.org/10.4049/jimmunol.1900443
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