Tissue Resident CCR2− and CCR2+ Cardiac Macrophages Differentially Orchestrate Monocyte Recruitment and Fate Specification Following Myocardial Injury
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Rationale: Recent advancements have brought to light the origins, complexity, and functions of tissue-resident macrophages. However, in the context of tissue injury or disease, large numbers of monocytes infiltrate the heart and are thought to contribute to adverse remodeling and heart failure pathogenesis. Little is understood about the diversity of monocytes and monocyte-derived macrophages recruited to the heart after myocardial injury, including the mechanisms that regulate monocyte recruitment and fate specification. Objective: We sought to test the hypothesis that distinct subsets of tissue-resident CCR2− (C-C chemokine receptor 2) and CCR2+ macrophages orchestrate monocyte recruitment and fate specification after myocardial injury. Methods and Results: We reveal that in numerous mouse models of cardiomyocyte cell death (permanent myocardial infarction, reperfused myocardial infarction, and diphtheria toxin cardiomyocyte ablation), there is a shift in macrophage ontogeny whereby tissue-resident macrophages are predominately replaced by infiltrating monocytes and monocyte-derived macrophages. Using syngeneic cardiac transplantation to model ischemia-reperfusion injury and distinguish tissue-resident from recruited cell populations in combination with intravital 2-photon microscopy, we demonstrate that monocyte recruitment is differentially orchestrated by distinct subsets of tissue-resident cardiac macrophages. Tissue-resident CCR2+ macrophages promote monocyte recruitment through an MYD88 (myeloid differentiation primary response 88)-dependent mechanism that results in release of MCPs (monocyte chemoattractant proteins) and monocyte mobilization. In contrast, tissue-resident CCR2− macrophages inhibit monocyte recruitment. Using CD (cluster of differentiation) 169-DTR (diphtheria toxin receptor) and CCR2-DTR mice, we further show that selective depletion of either tissue-resident CCR2− or CCR2+ macrophages before myocardial infarction results in divergent effects on left ventricular function, myocardial remodeling, and monocyte recruitment. Finally, using single-cell RNA sequencing, we show that tissue-resident cardiac macrophages differentially instruct monocyte fate specification. Conclusions: Collectively, these observations establish the mechanistic basis by which monocytes are initially recruited to the injured heart and provide new insights into the heterogeneity of monocyte-derived macrophages.
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IL-1β was selectively expressed by CCR2-positive monocytes and macrophages in the human heart.
“We demonstrated that IL-1β was selectively expressed by CCR2+ monocytes and macrophages in the human heart, consistent with our earlier mouse studies42,43.”
From Targeting immune–fibroblast cell communication in heart failure (2024) · cites this paper as [42]
The Results section on monocyte-derived macrophages reports higher Il1β expression in recruited CCR2+ macrophages from injured mouse hearts. It does not establish selective expression by CCR2+ monocytes and macrophages in the human heart; the paper mentions human cardiac macrophage subsets but does not report this IL-1β finding in humans. No page numbers are available in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIL-1β is selectively expressed by CCR2+ monocytes and macrophages in the human heart.
“We show that IL-1 β is selectively expressed by CCR2 + monocytes and macrophages in the human heart consistent with our prior mouse studies 37,38 .”
From Targeting the Immune-Fibrosis Axis in Myocardial Infarction and Heart Failure (2022) · cites this paper as [37]
The Results section on monocyte-derived macrophages reports higher Il1β expression in recruited CCR2+ macrophages from injured mouse hearts. That is consistent with the citing sentence’s reference to prior mouse studies, but this paper does not establish selective expression by both CCR2+ monocytes and macrophages in the human heart; no page number is available in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMyeloid clusters 1 and 5 highly expressed Ccr2, a marker of monocyte-derived macrophages that enter from the circulation.
“Clusters 1 and 5 had high expression of Ccr2, a marker of monocyte-derived macrophages that infiltrate from the circulation17-19 (Fig. 1J and Extended Data Fig. 1C-E).”
From Chromatin remodelling drives immune cell–fibroblast communication in heart failure (2024) · cites this paper as [19]
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Koenig, A. L., Kadyrov, F. F., Amrute, J. M., Yang, S., Weinheimer, C. J., Nigro, J. M., Kovacs, A., Smith, G., & Lavine, K. J. (2023) · doi:10.1101/2023.12.24.573263 · Cited by 12 · see citing works
Self-citationDefining Cardiac Recovery at Single Cell Resolution
Amrute, J. M., Lai, L., Ma, P., Koenig, A. L., Kamimoto, K., Bredemeyer, A., Shankar, T. S., Kuppe, C., Kadyrov, F. F., Schulte, L. J., et al. (2022) · doi:10.1101/2022.09.11.507463 · Cited by 6 · see citing works
Self-citationKadyrov, F. F., Koenig, A. L., Amrute, J. M., Dun, H., Li, W., Weinheimer, C. J., Nigro, J. M., Kovacs, A., Bredemeyer, A. L., Lai, L., et al. (2022) · doi:10.1101/2022.08.04.502542 · Cited by 3 · see citing works
Self-citation
- Authors
- Bajpai, G., Bredemeyer, A., Li, W., Zaitsev, K., Koenig, A. L., Lokshina, I., Mohan, J., Ivey, B., Hsiao, H.-M., Weinheimer, C., Kovacs, A., Epelman, S., Artyomov, M., Kreisel, D., & Lavine, K. J.
- Affiliations
- Washington University in St. Louis (US)
- From the Department of Medicine (G.B., A.B., A.L. Koenig, I.L., J.M., B.I., C.W., A. Kovacs, K.J.L.), Washington University School of Medicine, St. Louis, MO
- University Health Network (CA)
- Corresponding author
- Bajpai, Geetika
- Bredemeyer, Andrea
- ORCID
- Venue
- Circulation Research
- Published
- 2019-01-18
- Volume
- 124
- Issue
- 2
- Pages
- 263-278
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC6626616
- OpenAlex
- W2904624968
- Cited by
- 751
- References
- 58
- Citations by year
- 2026: 106 · 2025: 121 · 2024: 137 · 2023: 99 · 2022: 107 · 2021: 79 · 2020: 67 · 2019: 35
- FWCI
- 52.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX002730)
- National Heart, Lung, and Blood Institute (R01HL138466, R01HL139714, T32HL134635, K08HL123519, R01HL094601)
- National Institute of Allergy and Infectious Diseases (R21AI148877, P01AI116501)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK052574)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Keywords
- tissue-resident macrophages, CCR2, CCR2+ macrophages, monocyte recruitment, monocyte-derived macrophages, myocardial injury, myocardial infarction, ischemia-reperfusion injury, MyD88, monocyte chemoattractant protein, monocyte mobilization, macrophage ontogeny, macrophage heterogeneity, cardiac remodeling, left ventricular function
- MeSH terms
- Animals, Chemotaxis, Leukocyte, Diphtheria Toxin, Disease Models, Animal, Macrophage Activation, Macrophages, Mice, Inbred C57BL, Monocytes, Myocardial Infarction, Signal Transduction, Myocardial Reperfusion Injury, Heart Transplantation, Ventricular Function, Left, Cell Death, Mice, Knockout, Cell Lineage, Ventricular Remodeling, Myocytes, Cardiac, Myeloid Differentiation Factor 88, Receptors, CCR2
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