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Tracing LYVE1+ peritoneal fluid macrophages unveils two paths to resident macrophage repopulation with differing reliance on monocytes

Gallerand, A.; Han, J. J.; Mintz, R. L.; Chen, J.; Lee, D. D.; Chan, M. M.; Harmon, M. T.; Lin, X.; Huckstep, C. G.; Du, S.; Liu, T.; Kipnis, J.; Lavine, K. J.; Schilling, J.; Morley, S. C.; Zinselmeyer, B. H.; Randolph, G. J.

2025-03-19 immunology
10.1101/2025.03.19.644175 bioRxiv
Show abstract

Mouse resident peritoneal macrophages, called large cavity macrophages (LCM), arise from embryonic progenitors that proliferate as mature, CD73+Gata6+ tissue-specialized macrophages. After injury from irradiation or inflammation, monocytes are thought to replenish CD73+Gata6+ LCMs through a CD73-LYVE1+ LCM intermediate. Here, we show that CD73-LYVE1+ LCMs indeed yield Gata6+CD73+ LCMs through integrin-mediated interactions with mesothelial surfaces. CD73-LYVE1+ LCM repopulation of the peritoneum was reliant upon and quantitatively proportional to recruited monocytes. Unexpectedly, fate mapping indicated that only [~]10% of Gata6-dependent LCMs that repopulated the peritoneum after injury depended on the LYVE1+ LCM stage. Further supporting nonoverlapping lifecycles of CD73-LYVE1+ and CD73+Gata6+ LCMs, in mice bearing a paucity of monocytes, Gata6+CD73+ LCMs rebounded after ablative irradiation substantially more efficiently than their presumed LYVE1+ or CD73- LCM upstream precursors. Thus, after inflammatory insult, two temporally parallel pathways, each generating distinct differentiation intermediates with varying dependencies on monocytes, contribute to the replenish hment of Gata6+ resident peritoneal macrophages.

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