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A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish

Homeostatic trafficking to lymph nodes allows T cells to efficiently survey the host for cognate antigen. Nonmammalian jawed vertebrates lack lymph nodes but maintain diverse T cell pools. Here, we exploit in vivo imaging of transparent zebrafish to investigate how T cells organize and survey for an...

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Autores principales: Robertson, Tanner F., Hou, Yiran, Schrope, Jonathan, Shen, Simone, Rindy, Julie, Sauer, John-Demian, Dinh, Huy Q., Huttenlocher, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193988/
https://www.ncbi.nlm.nih.gov/pubmed/37155881
http://dx.doi.org/10.1073/pnas.2301137120
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author Robertson, Tanner F.
Hou, Yiran
Schrope, Jonathan
Shen, Simone
Rindy, Julie
Sauer, John-Demian
Dinh, Huy Q.
Huttenlocher, Anna
author_facet Robertson, Tanner F.
Hou, Yiran
Schrope, Jonathan
Shen, Simone
Rindy, Julie
Sauer, John-Demian
Dinh, Huy Q.
Huttenlocher, Anna
author_sort Robertson, Tanner F.
collection PubMed
description Homeostatic trafficking to lymph nodes allows T cells to efficiently survey the host for cognate antigen. Nonmammalian jawed vertebrates lack lymph nodes but maintain diverse T cell pools. Here, we exploit in vivo imaging of transparent zebrafish to investigate how T cells organize and survey for antigen in an animal devoid of lymph nodes. We find that naïve-like T cells in zebrafish organize into a previously undescribed whole-body lymphoid network that supports streaming migration and coordinated trafficking through the host. This network has the cellular hallmarks of a mammalian lymph node, including naïve T cells and CCR7-ligand expressing nonhematopoietic cells, and facilitates rapid collective migration. During infection, T cells transition to a random walk that supports antigen-presenting cell interactions and subsequent activation. Our results reveal that T cells can toggle between collective migration and individual random walks to prioritize either large-scale trafficking or antigen search in situ. This lymphoid network thus facilitates whole-body T cell trafficking and antigen surveillance in the absence of a lymph node system.
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spelling pubmed-101939882023-11-08 A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish Robertson, Tanner F. Hou, Yiran Schrope, Jonathan Shen, Simone Rindy, Julie Sauer, John-Demian Dinh, Huy Q. Huttenlocher, Anna Proc Natl Acad Sci U S A Biological Sciences Homeostatic trafficking to lymph nodes allows T cells to efficiently survey the host for cognate antigen. Nonmammalian jawed vertebrates lack lymph nodes but maintain diverse T cell pools. Here, we exploit in vivo imaging of transparent zebrafish to investigate how T cells organize and survey for antigen in an animal devoid of lymph nodes. We find that naïve-like T cells in zebrafish organize into a previously undescribed whole-body lymphoid network that supports streaming migration and coordinated trafficking through the host. This network has the cellular hallmarks of a mammalian lymph node, including naïve T cells and CCR7-ligand expressing nonhematopoietic cells, and facilitates rapid collective migration. During infection, T cells transition to a random walk that supports antigen-presenting cell interactions and subsequent activation. Our results reveal that T cells can toggle between collective migration and individual random walks to prioritize either large-scale trafficking or antigen search in situ. This lymphoid network thus facilitates whole-body T cell trafficking and antigen surveillance in the absence of a lymph node system. National Academy of Sciences 2023-05-08 2023-05-16 /pmc/articles/PMC10193988/ /pubmed/37155881 http://dx.doi.org/10.1073/pnas.2301137120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Robertson, Tanner F.
Hou, Yiran
Schrope, Jonathan
Shen, Simone
Rindy, Julie
Sauer, John-Demian
Dinh, Huy Q.
Huttenlocher, Anna
A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title_full A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title_fullStr A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title_full_unstemmed A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title_short A tessellated lymphoid network provides whole-body T cell surveillance in zebrafish
title_sort tessellated lymphoid network provides whole-body t cell surveillance in zebrafish
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193988/
https://www.ncbi.nlm.nih.gov/pubmed/37155881
http://dx.doi.org/10.1073/pnas.2301137120
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