Expansion of Pathogenic Cardiac Macrophages in Immune Checkpoint Inhibitor Myocarditis
Open accessAbstract
BACKGROUND: Immune checkpoint inhibitors (ICIs), antibodies targeting PD-1 (programmed cell death protein 1)/PD-L1 (programmed death-ligand 1) or CTLA4 (cytotoxic T-lymphocyte–associated protein 4), have revolutionized cancer management but are associated with devastating immune-related adverse events including myocarditis. The main risk factor for ICI myocarditis is the use of combination PD-1 and CTLA4 inhibition. ICI myocarditis is often fulminant and is pathologically characterized by myocardial infiltration of T lymphocytes and macrophages. Although much has been learned about the role of T-cells in ICI myocarditis, little is understood about the identity, transcriptional diversity, and functions of infiltrating macrophages. METHODS: We used an established murine ICI myocarditis model ( Ctla4 +/– Pdcd1 –/– mice) to explore the cardiac immune landscape using single-cell RNA-sequencing, immunostaining, flow cytometry, in situ RNA hybridization, molecular imaging, and antibody neutralization studies. RESULTS: We observed marked increases in CCR2 (C-C chemokine receptor type 2) + monocyte-derived macrophages and CD8 + T-cells in this model. The macrophage compartment was heterogeneous and displayed marked enrichment in an inflammatory CCR2 + subpopulation highly expressing Cxcl9 (chemokine [C-X-C motif] ligand 9), Cxcl10 (chemokine [C-X-C motif] ligand 10), Gbp2b (interferon-induced guanylate-binding protein 2b), and Fcgr4 (Fc receptor, IgG, low affinity IV) that originated from CCR2 + monocytes. It is important that a similar macrophage population expressing CXCL9 , CXCL10 , and CD16α (human homologue of mouse FcgR4) was expanded in patients with ICI myocarditis. In silico prediction of cell-cell communication suggested interactions between T-cells and Cxcl9 + Cxcl10 + macrophages via IFN-γ (interferon gamma) and CXCR3 (CXC chemokine receptor 3) signaling pathways. Depleting CD8 + T-cells or macrophages and blockade of IFN-γ signaling blunted the expansion of Cxcl9 + Cxcl10 + macrophages in the heart and attenuated myocarditis, suggesting that this interaction was necessary for disease pathogenesis. CONCLUSIONS: These data demonstrate that ICI myocarditis is associated with the expansion of a specific population of IFN-γ–induced inflammatory macrophages and suggest the possibility that IFN-γ blockade may be considered as a treatment option for this devastating condition.
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Macrophage-T-cell interaction is critical for the propagation of ICI myocarditis.
“with macrophage-T-cell interaction critical for its propagation.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
The Discussion describes a predicted feedback loop between T cells and inflammatory macrophages, and reports that depleting CD8+ T cells or macrophages improved survival in a mouse model of ICI myocarditis. But the proposed macrophage-to-T-cell signaling remains an informatic prediction; the paper does not establish that their interaction is critical for disease propagation. No page number is available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredDysregulation of cardiac macrophages plays a role in the pathogenesis of ICI myocarditis.
“a recent study demonstrated the dysregulation of cardiac macrophages playing a role in the pathogenesis of ICI myocarditis.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
In preclinical models of ICI myocarditis, T cells are necessary for the development of myocarditis.
“Data from preclinical models of ICI myocarditis suggested that T cells are necessary for the development of myocarditis”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
A recent study identified an expansion of a monocyte-derived Cxcl9+Cxcl10+ macrophage subset, induced by IFNγ signaling secreted by T lymphocytes, in ICI myocarditis.
“A recent study identified an expansion of a monocyte-derived Cxcl9 + Cxcl10 + macrophage subset, induced by IFNγ signaling secreted by T lymphocytes, in ICI myocarditis”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
Blocking IFNγ signaling or macrophage depletion reduced Cxcl9+Cxcl10+ macrophages and attenuated myocarditis in Ctla4+/-; Pdcd1-/- mice.
“blocking IFNγ signaling or macrophage depletion reduced Cxcl9 + Cxcl10 + macrophages and attenuated myocarditis in Ctla4+/-; Pdcd1 -/mice”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
In Ctla4+/-; Pdcd1-/- mice, elevated IFNγ levels promote differentiation of Cxcl9+Cxcl10+ inflammatory macrophages from CCR2+ monocytes in the heart.
“elevated IFNγ levels in Ctla4+/-; Pdcd1 -/mice, a mouse model for ICI myocarditis, promoted the differentiation of Cxcl9 + Cxcl10 + inflammatory macrophages from CCR2 + monocytes in the heart.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
Cxcl9+Cxcl10+ inflammatory macrophages are found in endomyocardial biopsies from ICI myocarditis.
“these macrophages were also found in EMB from ICI myocarditis.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [120]
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- Authors
- Ma, P., Liu, J., Qin, J., Lai, L., Heo, G. S., Luehmann, H., Sultan, D., Bredemeyer, A., Bajapa, G., Feng, G., Jimenez, J., He, R., Parks, A., Amrute, J., Villanueva, A., Liu, Y., Lin, C.-Y., Mack, M., Amancherla, K., Moslehi, J., & Lavine, K. J.
- Affiliations
- Washington University in St. Louis (US)
- University of California, San Francisco (US)
- Cardiovascular Division, Department of Medicine (P.M., J.L., A.B., G.B., G.F., J.J., R.H., A.P., J.A., K.J.L.), Washington University School of Medicine, St Louis, MO.
- University Hospital Regensburg (DE)
- Vanderbilt University Medical Center (US)
- ORCID
- Venue
- Circulation
- Published
- 2024-01-02
- Volume
- 149
- Issue
- 1
- Pages
- 48-66
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- PMC
- PMC11323830
- OpenAlex
- W4387001822
- Cited by
- 187
- References
- 53
- Citations by year
- 2026: 82 · 2025: 62 · 2024: 42 · 2023: 1
- FWCI
- 22.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- American Heart Association
- Fondation Leducq
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL138466, R01HL151078, R01HL139714, R01HL141466, R01HL150891, R01HL131908, R01HL153436, T32HL125241, R35HL161185, R01HL160688, R01HL156021, R35HL145212, R01HL151685, R01HL155990)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (P30AR073752)
- National Institute of Biomedical Imaging and Bioengineering (P41EB025815)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- immune checkpoint inhibitor-associated myocarditis, cardiac macrophages, CXCL9, CXCL10, CD8+ T cells, interferon-gamma signaling, macrophage heterogeneity, macrophage-T cell interaction, CTLA-4, PD-1, immune-related adverse events, chemokines, macrophage depletion
- MeSH terms
- Immune Checkpoint Inhibitors, Animals, Humans, Ligands, Macrophages, Myocarditis, RNA, CD8-Positive T-Lymphocytes, Chemokines, Mice, CTLA-4 Antigen, Programmed Cell Death 1 Receptor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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