Transcriptional and Immune Landscape of Cardiac Sarcoidosis
Open accessAbstract
Background: Cardiac involvement is an important determinant of mortality among sarcoidosis patients. Although granulomatous inflammation is a hallmark finding in cardiac sarcoidosis, the precise immune cell populations that comprise the granuloma remain unresolved. Furthermore, it is unclear how the cellular and transcriptomic landscape of cardiac sarcoidosis differs from other inflammatory heart diseases. Methods: We leveraged spatial transcriptomics (GeoMx digital spatial profiler) and single-nucleus RNA sequencing to elucidate the cellular and transcriptional landscape of cardiac sarcoidosis. Using GeoMX digital spatial profiler technology, we compared the transcriptomal profile of CD68 + rich immune cell infiltrates in human cardiac sarcoidosis, giant cell myocarditis, and lymphocytic myocarditis. We performed single-nucleus RNA sequencing of human cardiac sarcoidosis to identify immune cell types and examined their transcriptomic landscape and regulation. Using multichannel immunofluorescence staining, we validated immune cell populations identified by single-nucleus RNA sequencing, determined their spatial relationship, and devised an immunostaining approach to distinguish cardiac sarcoidosis from other inflammatory heart diseases. Results: Despite overlapping histological features, spatial transcriptomics identified transcriptional signatures and associated pathways that robustly differentiated cardiac sarcoidosis from giant cell myocarditis and lymphocytic myocarditis. Single-nucleus RNA sequencing revealed the presence of diverse populations of myeloid cells in cardiac sarcoidosis with distinct molecular features. We identified GPNMB (transmembrane glycoprotein NMB) as a novel marker of multinucleated giant cells and predicted that the MITF (microphthalmia-associated transcription factor) family of transcription factors regulated this cell type. We also detected additional macrophage populations in cardiac sarcoidosis including HLA-DR (human leukocyte antigen-DR) + macrophages, SYTL3 (synaptotagmin-like protein 3) + macrophages and CD163 + resident macrophages. HLA-DR + macrophages were found immediately adjacent to GPMMB + giant cells, a distinct feature compared with other inflammatory cardiac diseases. SYTL3 + macrophages were located scattered throughout the granuloma and CD163 + macrophages, CD1c + dendritic cells, nonclassical monocytes, and T cells were located at the periphery and outside of the granuloma. Finally, we demonstrate mTOR (mammalian target of rapamycin) pathway activation is associated with proliferation and is selectively found in HLA-DR + and SYLT3 + macrophages. Conclusions: In this study, we identified diverse populations of immune cells with distinct molecular signatures that comprise the sarcoid granuloma. These findings provide new insights into the pathology of cardiac sarcoidosis and highlight opportunities to improve diagnostic testing.
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Macrophages with heterogeneous origins constitute the largest immune cell population in giant cell myocarditis.
“macrophages, with heterogeneous origins, constituted the largest immune cell population in giant cell myocarditis”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [194]
The Results section (“Mac_GPNMB subcluster is specifically identified in cardiac sarcoidosis”; page unavailable) reports HLA-DR+ macrophages in giant cell myocarditis. It does not establish that macrophages are its largest immune-cell population or that they have heterogeneous origins; the paper’s analysis of distinct macrophage populations concerns cardiac sarcoidosis. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMultinucleated giant cells might originate from a particular macrophage subset expressing transmembrane GPNMB.
“multinucleated giant cells might originate from a particular macrophage subset expressing transmembrane GPNMB (glycoprotein NMB).”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [194]
The Results section on multinucleated giant cells suggests that Mac_SYTL3 macrophages could give rise to giant cells. It identifies the giant cells themselves as Mac_GPNMB, however, rather than identifying a GPNMB-expressing macrophage subset as their precursor. The Discussion describes GPNMB as a transmembrane protein. (LLM, conf=0.87)
Experimental — accuracy not yet measuredDistinct macrophage subsets from different origins contribute to sarcoidotic granuloma formation in the heart.
“distinct macrophage subsets from different origins contribute to sarcoidotic granuloma formation in the heart”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [194]
The Discussion (page not provided) reports distinct macrophage populations within cardiac sarcoid granulomas. It also says their origins are partly predicted and their exact roles in disease remain to be investigated; the paper does not establish that subsets from different origins drive granuloma formation. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn cardiac sarcoidosis, nonhematopoietic resident heart cells show a dysregulated transcription program including profibrotic proinflammatory fibroblasts, fibroblast-like angiogenic endothelial cells, and proinflammatory stress-related cardiomyocytes.
“a dysregulated transcription program in nonhematopoietic resident heart cells under conditions of cardiac sarcoidosis including profibrotic, proinflammatory fibroblasts; fibroblast-like, angiogenic endothelial cells; and proinflammatory, stressrelated cardiomyocytes.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [194]
The Results section on distinct transcriptomic signatures reports altered gene expression in CD68+ myeloid cells in cardiac sarcoidosis. It does not establish the claimed program in nonhematopoietic resident heart cells or the specified fibroblast, endothelial-cell, and cardiomyocyte phenotypes; searches for those cell types and phenotypes found no supporting passage. Page numbers were unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThese macrophages have upregulated mTOR signaling and alternative activation pathway and downregulated cytokine signaling and phagocytosis functions.
“with upregulated mTOR (mammalian target of rapamycin) signaling and alternative activation pathway as well as downregulated cytokine signaling and phagocytosis functions.”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [194]
The Results section on mTOR pathway activation reports upregulated mTOR-associated genes and high p-S6 staining in the Mac_HLA-DR and Mac_SYTL3 subsets, supporting increased mTOR activity in those macrophages, though staining varied across samples. Our copy does not report an upregulated alternative-activation pathway or downregulated cytokine signaling and phagocytosis functions; the Results section on multinucleated giant cells instead describes phagosome-pathway enrichment in several other myeloid subclusters. Page numbers are unavailable in our copy. (LLM, conf=0.87)
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Advances in cellular and tissue-based imaging techniques for sarcoid granulomas
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Cardiac sarcoidosis: new insights beyond the granuloma using spatial proteomics
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New insights gained from cellular landscape changes in myocarditis and inflammatory cardiomyopathy
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Positionspapier der ÖGR und ÖGP zur Diagnose und Therapie der Sarkoidose 2024
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Myopathology and Immune Profile of Granulomatous Myositis in Sarcoid Myopathy
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Is it Time to Incorporate Genomic Data in the Routine Evaluation of Cardiac Sarcoidosis?
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Cardiovascular Manifestations and Immunobiology of Sarcoidosis
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Integrated DNA methylome and transcriptome signatures of lung CD4 + T-cells in sarcoidosis
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Integrative Molecular Analyses of Inflammatory and Autoimmune Signals in Cardiac Sarcoidosis
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Leveraging Human Tissue for Discovery in Heart Transplantation
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MALDI-MSI reveals shared lipid signatures in sarcoid-like granulomas of mice and in a human case
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- Authors
- Liu, J., Ma, P., Lai, L., Villanueva, A., Koenig, A., Bean, G. R., Bowles, D. E., Glass, C., Watson, M., Lavine, K. J., & Lin, C.-Y.
- Affiliations
- Washington University in St. Louis (US)
- Stanford Medicine (US)
- Duke University (US)
- Corresponding author
- Liu, Jing
- Ma, Pan
- ORCID
- Venue
- Circulation Research
- Published
- 2022-09-30
- Volume
- 131
- Issue
- 8
- Pages
- 654-669
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC9514756
- OpenAlex
- W4296029945
- Cited by
- 78
- References
- 44
- Citations by year
- 2026: 20 · 2025: 22 · 2024: 20 · 2023: 15 · 2022: 1
- FWCI
- 8.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Circulation Research (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
- Funders
- National Institutes of Health (UL1TR002345)
- National Heart, Lung, and Blood Institute (R01HL138466, R01HL151078, R01HL139714, T32HL125241, R35HL161185)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (P30AR073752)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Physiology › Sarcoidosis and Beryllium Toxicity Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- cardiac sarcoidosis, giant cell myocarditis, lymphocytic myocarditis, granuloma, myeloid cells, macrophage heterogeneity, multinucleated giant cells, GPNMB, MITF, mTOR signaling
- MeSH terms
- Granuloma, HLA Antigens, Humans, Membrane Glycoproteins, Myocarditis, Sarcoidosis, Synaptotagmins, Microphthalmia-Associated Transcription Factor, TOR Serine-Threonine Kinases
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