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Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish
Immune cells congregate at specific loci to fight infections during inflammatory responses, a process that must be transient and self-resolving. Cell dispersal promotes resolution, but it remains unclear how transition from clustering to dispersal is regulated. Here we show, using quantitative live...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6856356/ https://www.ncbi.nlm.nih.gov/pubmed/31727891 http://dx.doi.org/10.1038/s41467-019-13107-3 |
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author | Coombs, Caroline Georgantzoglou, Antonios Walker, Hazel A. Patt, Julian Merten, Nicole Poplimont, Hugo Busch-Nentwich, Elisabeth M. Williams, Sarah Kotsi, Christina Kostenis, Evi Sarris, Milka |
author_facet | Coombs, Caroline Georgantzoglou, Antonios Walker, Hazel A. Patt, Julian Merten, Nicole Poplimont, Hugo Busch-Nentwich, Elisabeth M. Williams, Sarah Kotsi, Christina Kostenis, Evi Sarris, Milka |
author_sort | Coombs, Caroline |
collection | PubMed |
description | Immune cells congregate at specific loci to fight infections during inflammatory responses, a process that must be transient and self-resolving. Cell dispersal promotes resolution, but it remains unclear how transition from clustering to dispersal is regulated. Here we show, using quantitative live imaging in zebrafish, that differential ligand-induced trafficking of chemokine receptors such as Cxcr1 and Cxcr2 orchestrates the state of neutrophil congregation at sites of tissue damage. Through receptor mutagenesis and biosensors, we show that Cxcr1 promotes clustering at wound sites, but is promptly desensitized and internalized, which prevents excess congregation. By contrast, Cxcr2 promotes bidirectional motility and is sustained at the plasma membrane. Persistent plasma membrane residence of Cxcr2 prolongs downstream signaling and is required for sustained exploratory motion conducive to dispersal. Thus, differential trafficking of two chemokine receptors allows coordination of antagonistic cell behaviors, promoting a self-resolving migratory response. |
format | Online Article Text |
id | pubmed-6856356 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-68563562019-11-18 Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish Coombs, Caroline Georgantzoglou, Antonios Walker, Hazel A. Patt, Julian Merten, Nicole Poplimont, Hugo Busch-Nentwich, Elisabeth M. Williams, Sarah Kotsi, Christina Kostenis, Evi Sarris, Milka Nat Commun Article Immune cells congregate at specific loci to fight infections during inflammatory responses, a process that must be transient and self-resolving. Cell dispersal promotes resolution, but it remains unclear how transition from clustering to dispersal is regulated. Here we show, using quantitative live imaging in zebrafish, that differential ligand-induced trafficking of chemokine receptors such as Cxcr1 and Cxcr2 orchestrates the state of neutrophil congregation at sites of tissue damage. Through receptor mutagenesis and biosensors, we show that Cxcr1 promotes clustering at wound sites, but is promptly desensitized and internalized, which prevents excess congregation. By contrast, Cxcr2 promotes bidirectional motility and is sustained at the plasma membrane. Persistent plasma membrane residence of Cxcr2 prolongs downstream signaling and is required for sustained exploratory motion conducive to dispersal. Thus, differential trafficking of two chemokine receptors allows coordination of antagonistic cell behaviors, promoting a self-resolving migratory response. Nature Publishing Group UK 2019-11-14 /pmc/articles/PMC6856356/ /pubmed/31727891 http://dx.doi.org/10.1038/s41467-019-13107-3 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
spellingShingle | Article Coombs, Caroline Georgantzoglou, Antonios Walker, Hazel A. Patt, Julian Merten, Nicole Poplimont, Hugo Busch-Nentwich, Elisabeth M. Williams, Sarah Kotsi, Christina Kostenis, Evi Sarris, Milka Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title | Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title_full | Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title_fullStr | Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title_full_unstemmed | Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title_short | Chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
title_sort | chemokine receptor trafficking coordinates neutrophil clustering and dispersal at wounds in zebrafish |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6856356/ https://www.ncbi.nlm.nih.gov/pubmed/31727891 http://dx.doi.org/10.1038/s41467-019-13107-3 |
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