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Prostaglandin E2 controls the metabolic adaptation of T cells to the intestinal microenvironment

Villa, M.; Sanin, D. E.; Apostolova, P.; Corrado, M.; Kabat, A. M.; Cristinzio, C.; Regina, A.; Carrizo, G.; Rana, N.; Stanczak, M. A.; Baixauli, F.; Grzes, K. M.; Cupovic, J.; Solagna, F.; Hackl, A.; Globig, A.-M.; Haessler, F.; Puleston, D. J.; Kelly, B.; Cabezas-Wallscheid, N.; Hasselblatt, P.; Bengsch, B.; Zeiser, R.; Sagar, ; Buescher, J. M.; Pearce, E. J.; Pearce, E. L.

2023-03-15 immunology
10.1101/2023.03.13.532431 bioRxiv
Show abstract

Immune cells must adapt to different environments during the course of an immune response. We studied the adaptation of CD8+ T cells to the intestinal microenvironment and how this process shapes their residency in the gut. CD8+ T cells progressively remodel their transcriptome and surface phenotype as they acquire gut residency, and downregulate expression of mitochondrial genes. Human and mouse gut-resident CD8+ T cells have reduced mitochondrial mass, but maintain a viable energy balance to sustain their function. We found that the intestinal microenvironment is rich in prostaglandin E2 (PGE2), which drives mitochondrial depolarization in CD8+ T cells. Consequently, these cells engage autophagy to clear depolarized mitochondria, and enhance glutathione synthesis to scavenge reactive oxygen species (ROS) that result from mitochondrial depolarization. Impairing PGE2 sensing promotes CD8+ T cell accumulation in the gut, while tampering with autophagy and glutathione negatively impacts the T cell population. Thus, a PGE2-autophagy-glutathione axis defines the metabolic adaptation of CD8+ T cells to the intestinal microenvironment, to ultimately influence the T cell pool.

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