Cargando…

Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod

As the lowest organisms possessing T cells, fish are instrumental for understanding T cell evolution and immune defense in early vertebrates. This study established in Nile tilapia models suggests that T cells play a critical role in resisting Edwardsiella piscicida infection via cytotoxicity and ar...

Descripción completa

Detalles Bibliográficos
Autores principales: Li, Kang, Wei, Xiumei, Jiao, Xinying, Deng, Wenhai, Li, Jiaqi, Liang, Wei, Zhang, Yu, Yang, Jialong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10131875/
https://www.ncbi.nlm.nih.gov/pubmed/36890649
http://dx.doi.org/10.1002/advs.202201164
_version_ 1785031274238312448
author Li, Kang
Wei, Xiumei
Jiao, Xinying
Deng, Wenhai
Li, Jiaqi
Liang, Wei
Zhang, Yu
Yang, Jialong
author_facet Li, Kang
Wei, Xiumei
Jiao, Xinying
Deng, Wenhai
Li, Jiaqi
Liang, Wei
Zhang, Yu
Yang, Jialong
author_sort Li, Kang
collection PubMed
description As the lowest organisms possessing T cells, fish are instrumental for understanding T cell evolution and immune defense in early vertebrates. This study established in Nile tilapia models suggests that T cells play a critical role in resisting Edwardsiella piscicida infection via cytotoxicity and are essential for IgM(+) B cell response. CD3 and CD28 monoclonal antibody crosslinking reveals that full activation of tilapia T cells requires the first and secondary signals, while Ca(2+)–NFAT, MAPK/ERK, NF‐κB, and mTORC1 pathways and IgM(+) B cells collectively regulate T cell activation. Thus, despite the large evolutionary distance, tilapia and mammals such as mice and humans exhibit similar T cell functions. Furthermore, it is speculated that transcriptional networks and metabolic reprogramming, especially c‐Myc‐mediated glutamine metabolism triggered by mTORC1 and MAPK/ERK pathways, underlie the functional similarity of T cells between tilapia and mammals. Notably, tilapia, frogs, chickens, and mice utilize the same mechanisms to facilitate glutaminolysis‐regulated T cell responses, and restoration of the glutaminolysis pathway using tilapia components rescues the immunodeficiency of human Jurkat T cells. Thus, this study provides a comprehensive picture of T cell immunity in tilapia, sheds novel perspectives for understanding T cell evolution, and offers potential avenues for intervening in human immunodeficiency.
format Online
Article
Text
id pubmed-10131875
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-101318752023-04-27 Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod Li, Kang Wei, Xiumei Jiao, Xinying Deng, Wenhai Li, Jiaqi Liang, Wei Zhang, Yu Yang, Jialong Adv Sci (Weinh) Research Articles As the lowest organisms possessing T cells, fish are instrumental for understanding T cell evolution and immune defense in early vertebrates. This study established in Nile tilapia models suggests that T cells play a critical role in resisting Edwardsiella piscicida infection via cytotoxicity and are essential for IgM(+) B cell response. CD3 and CD28 monoclonal antibody crosslinking reveals that full activation of tilapia T cells requires the first and secondary signals, while Ca(2+)–NFAT, MAPK/ERK, NF‐κB, and mTORC1 pathways and IgM(+) B cells collectively regulate T cell activation. Thus, despite the large evolutionary distance, tilapia and mammals such as mice and humans exhibit similar T cell functions. Furthermore, it is speculated that transcriptional networks and metabolic reprogramming, especially c‐Myc‐mediated glutamine metabolism triggered by mTORC1 and MAPK/ERK pathways, underlie the functional similarity of T cells between tilapia and mammals. Notably, tilapia, frogs, chickens, and mice utilize the same mechanisms to facilitate glutaminolysis‐regulated T cell responses, and restoration of the glutaminolysis pathway using tilapia components rescues the immunodeficiency of human Jurkat T cells. Thus, this study provides a comprehensive picture of T cell immunity in tilapia, sheds novel perspectives for understanding T cell evolution, and offers potential avenues for intervening in human immunodeficiency. John Wiley and Sons Inc. 2023-03-08 /pmc/articles/PMC10131875/ /pubmed/36890649 http://dx.doi.org/10.1002/advs.202201164 Text en © 2023 The Authors. Advanced Science published by Wiley‐VCH GmbH https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Li, Kang
Wei, Xiumei
Jiao, Xinying
Deng, Wenhai
Li, Jiaqi
Liang, Wei
Zhang, Yu
Yang, Jialong
Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title_full Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title_fullStr Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title_full_unstemmed Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title_short Glutamine Metabolism Underlies the Functional Similarity of T Cells between Nile Tilapia and Tetrapod
title_sort glutamine metabolism underlies the functional similarity of t cells between nile tilapia and tetrapod
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10131875/
https://www.ncbi.nlm.nih.gov/pubmed/36890649
http://dx.doi.org/10.1002/advs.202201164
work_keys_str_mv AT likang glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT weixiumei glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT jiaoxinying glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT dengwenhai glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT lijiaqi glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT liangwei glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT zhangyu glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod
AT yangjialong glutaminemetabolismunderliesthefunctionalsimilarityoftcellsbetweenniletilapiaandtetrapod