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Pioneer neutrophils release chromatin within in vivo swarms

Neutrophils are rapidly recruited to inflammatory sites where their coordinated migration forms clusters, a process termed neutrophil swarming. The factors that modulate early stages of neutrophil swarming are not fully understood, requiring the development of new in vivo models. Using transgenic ze...

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Autores principales: Isles, Hannah M, Loynes, Catherine A, Alasmari, Sultan, Kon, Fu Chuen, Henry, Katherine M, Kadochnikova, Anastasia, Hales, Jack, Muir, Clare F, Keightley, Maria-Cristina, Kadirkamanathan, Visakan, Hamilton, Noémie, Lieschke, Graham J, Renshaw, Stephen A, Elks, Philip M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8298094/
https://www.ncbi.nlm.nih.gov/pubmed/34292151
http://dx.doi.org/10.7554/eLife.68755
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author Isles, Hannah M
Loynes, Catherine A
Alasmari, Sultan
Kon, Fu Chuen
Henry, Katherine M
Kadochnikova, Anastasia
Hales, Jack
Muir, Clare F
Keightley, Maria-Cristina
Kadirkamanathan, Visakan
Hamilton, Noémie
Lieschke, Graham J
Renshaw, Stephen A
Elks, Philip M
author_facet Isles, Hannah M
Loynes, Catherine A
Alasmari, Sultan
Kon, Fu Chuen
Henry, Katherine M
Kadochnikova, Anastasia
Hales, Jack
Muir, Clare F
Keightley, Maria-Cristina
Kadirkamanathan, Visakan
Hamilton, Noémie
Lieschke, Graham J
Renshaw, Stephen A
Elks, Philip M
author_sort Isles, Hannah M
collection PubMed
description Neutrophils are rapidly recruited to inflammatory sites where their coordinated migration forms clusters, a process termed neutrophil swarming. The factors that modulate early stages of neutrophil swarming are not fully understood, requiring the development of new in vivo models. Using transgenic zebrafish larvae to study endogenous neutrophil migration in a tissue damage model, we demonstrate that neutrophil swarming is a conserved process in zebrafish immunity, sharing essential features with mammalian systems. We show that neutrophil swarms initially develop around an individual pioneer neutrophil. We observed the violent release of extracellular cytoplasmic and nuclear fragments by the pioneer and early swarming neutrophils. By combining in vitro and in vivo approaches to study essential components of neutrophil extracellular traps (NETs), we provide in-depth characterisation and high-resolution imaging of the composition and morphology of these release events. Using a photoconversion approach to track neutrophils within developing swarms, we identify that the fate of swarm-initiating pioneer neutrophils involves extracellular chromatin release and that the key NET components gasdermin, neutrophil elastase, and myeloperoxidase are required for the swarming process. Together our findings demonstrate that release of cellular components by pioneer neutrophils is an initial step in neutrophil swarming at sites of tissue injury.
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spelling pubmed-82980942021-07-23 Pioneer neutrophils release chromatin within in vivo swarms Isles, Hannah M Loynes, Catherine A Alasmari, Sultan Kon, Fu Chuen Henry, Katherine M Kadochnikova, Anastasia Hales, Jack Muir, Clare F Keightley, Maria-Cristina Kadirkamanathan, Visakan Hamilton, Noémie Lieschke, Graham J Renshaw, Stephen A Elks, Philip M eLife Immunology and Inflammation Neutrophils are rapidly recruited to inflammatory sites where their coordinated migration forms clusters, a process termed neutrophil swarming. The factors that modulate early stages of neutrophil swarming are not fully understood, requiring the development of new in vivo models. Using transgenic zebrafish larvae to study endogenous neutrophil migration in a tissue damage model, we demonstrate that neutrophil swarming is a conserved process in zebrafish immunity, sharing essential features with mammalian systems. We show that neutrophil swarms initially develop around an individual pioneer neutrophil. We observed the violent release of extracellular cytoplasmic and nuclear fragments by the pioneer and early swarming neutrophils. By combining in vitro and in vivo approaches to study essential components of neutrophil extracellular traps (NETs), we provide in-depth characterisation and high-resolution imaging of the composition and morphology of these release events. Using a photoconversion approach to track neutrophils within developing swarms, we identify that the fate of swarm-initiating pioneer neutrophils involves extracellular chromatin release and that the key NET components gasdermin, neutrophil elastase, and myeloperoxidase are required for the swarming process. Together our findings demonstrate that release of cellular components by pioneer neutrophils is an initial step in neutrophil swarming at sites of tissue injury. eLife Sciences Publications, Ltd 2021-07-21 /pmc/articles/PMC8298094/ /pubmed/34292151 http://dx.doi.org/10.7554/eLife.68755 Text en © 2021, Isles et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Immunology and Inflammation
Isles, Hannah M
Loynes, Catherine A
Alasmari, Sultan
Kon, Fu Chuen
Henry, Katherine M
Kadochnikova, Anastasia
Hales, Jack
Muir, Clare F
Keightley, Maria-Cristina
Kadirkamanathan, Visakan
Hamilton, Noémie
Lieschke, Graham J
Renshaw, Stephen A
Elks, Philip M
Pioneer neutrophils release chromatin within in vivo swarms
title Pioneer neutrophils release chromatin within in vivo swarms
title_full Pioneer neutrophils release chromatin within in vivo swarms
title_fullStr Pioneer neutrophils release chromatin within in vivo swarms
title_full_unstemmed Pioneer neutrophils release chromatin within in vivo swarms
title_short Pioneer neutrophils release chromatin within in vivo swarms
title_sort pioneer neutrophils release chromatin within in vivo swarms
topic Immunology and Inflammation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8298094/
https://www.ncbi.nlm.nih.gov/pubmed/34292151
http://dx.doi.org/10.7554/eLife.68755
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