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AMPK activation induces RALDHhigh tolerogenic dendritic cells through rewiring of glucose and lipid metabolism

Brombacher, E. C.; Patente, T. A.; van der Ham, A. J.; Moll, T. J. A.; Otto, F.; Verheijen, F. W. M.; Zaal, E. A.; de Ru, A. H.; Tjokrodirijo, R. T. N.; Berkers, C. R.; van Veelen, P. A.; Guigas, B.; Everts, B.

2023-07-04 immunology
10.1101/2023.07.04.547639 bioRxiv
Show abstract

It is well known that dendritic cell (DC) activation and function are underpinned by profound changes in cellular metabolism. Several studies indicate that the ability of DCs to promote tolerance is dependent on catabolic metabolism. The AMP-activated kinase (AMPK) is a central nutrient and energy sensor whose activation promotes catabolism while inhibiting ATP-consuming anabolic pathways. Yet the contribution of AMPK activation to DC tolerogenicity remains unknown. Here, we show that AMPK activation renders human monocyte-derived DCs tolerogenic as evidenced by an enhanced ability to drive differentiation of regulatory T cells, a process dependent on increased RALDH activity. This is accompanied by a number of distinct metabolic changes, in particular increased breakdown of glycerophospholipids, enhanced mitochondrial fission-dependent fatty acid oxidation, and upregulated glucose catabolism. This metabolic rewiring is functionally important as we found interference with these metabolic processes to reduce to various degrees AMPK-induced RALDH activity as well as the tolerogenic capacity of moDCs. Altogether, our findings reveal a key role for AMPK signaling in shaping DC tolerogenicity, and suggest that AMPK may serve as new target to direct DC-driven immune responses in therapeutic settings.

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