Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1783449678499545088 |
---|---|
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. |
format | Online Article Text |
id | pubmed-6731454 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | AAI |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT mccormickbarry anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT craighelene anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT chujuliay anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT carlinleom anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT canelmarta anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT wollweberflorian anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT toivakkamatilda anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT michaelmelina anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT astierannel anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT nortonlaura anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT liljajohanna anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT feltonjenniferm anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT sasakitakehiko anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT ivaskajohanna anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT hersingeborg anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT dransfieldian anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT rossiadrianog anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT vermerensonja anegativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT mccormickbarry negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT craighelene negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT chujuliay negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT carlinleom negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT canelmarta negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT wollweberflorian negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT toivakkamatilda negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT michaelmelina negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT astierannel negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT nortonlaura negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT liljajohanna negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT feltonjenniferm negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT sasakitakehiko negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT ivaskajohanna negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT hersingeborg negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT dransfieldian negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT rossiadrianog negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites AT vermerensonja negativefeedbackloopregulatesintegrininactivationandpromotesneutrophilrecruitmenttoinflammatorysites |