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

Author:

Li Kang12,Wei Xiumei12,Jiao Xinying12,Deng Wenhai3,Li Jiaqi12,Liang Wei12,Zhang Yu1,Yang Jialong12ORCID

Affiliation:

1. State Key Laboratory of Estuarine and Coastal Research School of Life Sciences East China Normal University Shanghai 200241 China

2. Laboratory for Marine Biology and Biotechnology Qingdao National Laboratory for Marine Science and Technology Qingdao 266237 China

3. School of Laboratory Medicine and Life Science Wenzhou Medical University Wenzhou Zhejiang 325035 China

Abstract

AbstractAs 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 Ca2+–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.

Funder

National Natural Science Foundation of China

Natural Science Foundation of Shanghai

Publisher

Wiley

Subject

General Physics and Astronomy,General Engineering,Biochemistry, Genetics and Molecular Biology (miscellaneous),General Materials Science,General Chemical Engineering,Medicine (miscellaneous)

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