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Dick, Sarah A; Macklin, Jillian A; Nejat, Sara; Momen, Abdul; Clemente-Casares, Xavier; Althagafi, Marwan G; Chen, Jinmiao; Kantores, Crystal; Hosseinzadeh, Siyavash; Aronoff, Laura; Wong, Anthony; Zaman, Rysa; Barbu, Iulia; Besla, Rickvinder; Lavine, Kory J; Razani, Babak; Ginhoux, Florent; Husain, Mansoor; Cybulsky, Myron I; Robbins, Clinton S; Epelman, Slava
Nature immunology, 01/2019, Volume: 20, Issue: 1Journal Article
Macrophages promote both injury and repair after myocardial infarction, but discriminating functions within mixed populations remains challenging. Here we used fate mapping, parabiosis and single-cell transcriptomics to demonstrate that at steady state, TIMD4 LYVE1 MHC-II CCR2 resident cardiac macrophages self-renew with negligible blood monocyte input. Monocytes partially replaced resident TIMD4 LYVE1 MHC-II CCR2 macrophages and fully replaced TIMD4 LYVE1 MHC-II CCR2 macrophages, revealing a hierarchy of monocyte contribution to functionally distinct macrophage subsets. Ischemic injury reduced TIMD4 and TIMD4 resident macrophage abundance, whereas CCR2 monocyte-derived macrophages adopted multiple cell fates within infarcted tissue, including those nearly indistinguishable from resident macrophages. Recruited macrophages did not express TIMD4, highlighting the ability of TIMD4 to track a subset of resident macrophages in the absence of fate mapping. Despite this similarity, inducible depletion of resident macrophages using a Cx3cr1-based system led to impaired cardiac function and promoted adverse remodeling primarily within the peri-infarct zone, revealing a nonredundant, cardioprotective role of resident cardiac macrophages.
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