Mechanisms of epigenomic and functional convergence between glucocorticoid- and IL4-driven macrophage programming

Abstract Macrophages adopt distinct phenotypes in response to environmental cues, with type-2 cytokine interleukin-4 promoting a tissue-repair homeostatic state (M2IL4). Glucocorticoids (GC), widely used anti-inflammatory therapeutics, reportedly impart a similar phenotype (M2GC), but how such dispa...

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Main Authors: Dinesh K. Deochand, Marija Dacic, Michael J. Bale, Andrew W. Daman, Vidyanath Chaudhary, Steven Z. Josefowicz, David Oliver, Yurii Chinenov, Inez Rogatsky
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-52942-x
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Summary:Abstract Macrophages adopt distinct phenotypes in response to environmental cues, with type-2 cytokine interleukin-4 promoting a tissue-repair homeostatic state (M2IL4). Glucocorticoids (GC), widely used anti-inflammatory therapeutics, reportedly impart a similar phenotype (M2GC), but how such disparate pathways may functionally converge is unknown. We show using integrative functional genomics that M2IL4 and M2GC transcriptomes share a striking overlap mirrored by a shift in chromatin landscape in both common and signal-specific gene subsets. This core homeostatic program is enacted by transcriptional effectors KLF4 and the glucocorticoid receptor, whose genome-wide occupancy and actions are integrated in a stimulus-specific manner by the nuclear receptor cofactor GRIP1. Indeed, many of the M2IL4:M2GC-shared transcriptomic changes were GRIP1-dependent. Consistently, GRIP1 loss attenuated phagocytic activity of both populations in vitro and macrophage tissue-repair properties in the murine colitis model in vivo. These findings provide a mechanistic framework for homeostatic macrophage programming by distinct signals, to better inform anti-inflammatory drug design.
ISSN:2041-1723