Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
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
_version_ 1783470563109371904
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
work_keys_str_mv AT coombscaroline chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT georgantzoglouantonios chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT walkerhazela chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT pattjulian chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT mertennicole chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT poplimonthugo chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT buschnentwichelisabethm chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT williamssarah chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT kotsichristina chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT kostenisevi chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish
AT sarrismilka chemokinereceptortraffickingcoordinatesneutrophilclusteringanddispersalatwoundsinzebrafish