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Dietary restriction to optimize T cell immunity is an ancient survival strategy conserved in vertebrate evolution

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Abstract

Recent advances highlight a key role of transient fasting in optimizing immunity of human and mouse. However, it remains unknown whether this strategy is independently acquired by mammals during evolution or instead represents gradually evolved functions common to vertebrates. Using a tilapia model, we report that T cells are the main executors of the response of the immune system to fasting and that dietary restriction bidirectionally modulates T cell immunity. Long-term fasting impaired T cell immunity by inducing intense autophagy, apoptosis, and aberrant inflammation. However, transient dietary restriction triggered moderate autophagy to optimize T cell response by maintaining homeostasis, alleviating inflammation and tissue damage, as well as enhancing T cell activation, proliferation and function. Furthermore, AMPK is the central hub linking fasting and autophagy-controlled T cell immunity in tilapia. Our findings demonstrate that dietary restriction to optimize immunity is an ancient strategy conserved in vertebrate evolution, providing novel perspectives for understanding the adaptive evolution of T cell response.

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Acknowledgements

We thank the Instrument-sharing Platform of the School of Life Sciences of East China Normal University (ECNU) for instrument sharing, the Flow Cytometry Core Facility of the School of Life Sciences of ECNU for the FACS analysis.

Funding

This research was supported by grants from National Natural Science Foundation of China to Dr. Jialong Yang (no. 32022086) and Dr. Xiumei Wei (no. 31972822); and Natural Science Foundation of Shanghai to Dr. Xiumei Wei (no. 20ZR1417500).

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KML designed and performed experiments, analyzed data, and drafted the manuscript. XW acquired funding, conceived and administrated the project. KL, QZ and JZ performed experiments. DW kept the experimental animals. JY acquired funding, conceived the project, designed experiments, analyzed data, and drafted the manuscript.

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Correspondence to Jialong Yang.

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All animal experiments were conducted in accordance with the guidelines for the Care and Use of Laboratory Animals of the Ministry of Science and Technology of China, and approved by the East China Normal University Experimental Animal Ethics Committee with an approve number of AR2021-247. All efforts were made to minimize the pain of animals.

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Li, K., Wei, X., Li, K. et al. Dietary restriction to optimize T cell immunity is an ancient survival strategy conserved in vertebrate evolution. Cell. Mol. Life Sci. 80, 219 (2023). https://doi.org/10.1007/s00018-023-04865-x

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