Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis

Florian Leuschner, Philipp J. Rauch, Takuya Ueno, Rostic Gorbatov, Brett Marinelli, Won Woo Lee, Partha Dutta, Ying Wei, Clinton Robbins, Yoshiko Iwamoto, Brena Sena, Aleksey Chudnovskiy, Peter Panizzi, Edmund Keliher, John M. Higgins, Peter Libby, Michael A. Moskowitz, Mikael J. Pittet, Filip K. Swirski, Ralph WeisslederMatthias Nahrendorf

Research output: Contribution to journalArticlepeer-review

413 Scopus citations

Abstract

Monocytes (Mo) and macrophages (MΦ) are emerging therapeutic targets in malignant, cardiovascular, and autoimmune disorders. Targeting of Mo/MΦ and their effector functions without compromising innate immunity's critical defense mechanisms first requires addressing gaps in knowledge about the life cycle of these cells. Here we studied the source, tissue kinetics, and clearance of Mo/MΦ in murine myocardial infarction, a model of acute inflammation after ischemic injury. We found that a) Mo tissue residence time was surprisingly short (20 h); b) Mo recruitment rates were consistently high even days after initiation of inflammation; c) the sustained need of newly made Mo was fostered by extramedullary monocytopoiesis in the spleen; d) splenic monocytopoiesis was regulated by IL-1β; and e) the balance of cell recruitment and local death shifted during resolution of inflammation. Depending on the experimental approach, we measured a 24 h Mo/M exit rate from infarct tissue between 5 and 13% of the tissue cell population. Exited cells were most numerous in the blood, liver, and spleen. Abrogation of extramedullary monocytopoiesis proved deleterious for infarct healing and accelerated the evolution of heart failure. We also detected rapid Mo kinetics in mice with stroke. These findings expand our knowledge of Mo/MΦ flux in acute inflammation and provide the groundwork for novel anti-inflammatory strategies for treating heart failure.

Original languageEnglish
Pages (from-to)123-137
Number of pages15
JournalJournal of Experimental Medicine
Volume209
Issue number1
DOIs
StatePublished - Jan 2012
Externally publishedYes

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