A Novel Circulating Noncoding Small RNA for the Detection of Acute Myocarditis
Open accessAbstract
BACKGROUND: The diagnosis of acute myocarditis typically requires either endomyocardial biopsy (which is invasive) or cardiovascular magnetic resonance imaging (which is not universally available). Additional approaches to diagnosis are desirable. We sought to identify a novel microRNA for the diagnosis of acute myocarditis. METHODS: To identify a microRNA specific for myocarditis, we performed microRNA microarray analyses and quantitative polymerase-chain-reaction (qPCR) assays in sorted CD4+ T cells and type 17 helper T (Th17) cells after inducing experimental autoimmune myocarditis or myocardial infarction in mice. We also performed qPCR in samples from coxsackievirus-induced myocarditis in mice. We then identified the human homologue for this microRNA and compared its expression in plasma obtained from patients with acute myocarditis with the expression in various controls. RESULTS: We confirmed that Th17 cells, which are characterized by the production of interleukin-17, are a characteristic feature of myocardial injury in the acute phase of myocarditis. The microRNA mmu-miR-721 was synthesized by Th17 cells and was present in the plasma of mice with acute autoimmune or viral myocarditis but not in those with acute myocardial infarction. The human homologue, designated hsa-miR-Chr8:96, was identified in four independent cohorts of patients with myocarditis. The area under the receiver-operating-characteristic curve for this novel microRNA for distinguishing patients with acute myocarditis from those with myocardial infarction was 0.927 (95% confidence interval, 0.879 to 0.975). The microRNA retained its diagnostic value in models after adjustment for age, sex, ejection fraction, and serum troponin level. CONCLUSIONS: After identifying a novel microRNA in mice and humans with myocarditis, we found that the human homologue (hsa-miR-Chr8:96) could be used to distinguish patients with myocarditis from those with myocardial infarction. (Funded by the Spanish Ministry of Science and Innovation and others.).
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IL-1β increases serum and cardiac IL-6 levels that are needed to drive Th17 responses, which promote fibrosis and progression to DCM and heart failure in patients with myocarditis and in animal models.
“IL-1 β also increases serum and cardiac IL-6 levels that are needed to drive Th17 responses, which also promote fibrosis and progression to DCM and heart failure in patients with myocarditis and in animal models. 36,165,172-174”
From COVID-19, Myocarditis and Pericarditis (2023) · cites this paper as [173]
The Results section on Th17-specific responses (page not provided) reports increased Th17 cells in patients with acute myocarditis and in mouse models, alongside reduced ejection fraction. It does not show that IL-1β raises serum or cardiac IL-6, that IL-6 is needed to drive Th17 responses, or that those responses cause fibrosis or progression to dilated cardiomyopathy and heart failure. (LLM, conf=0.84)
Experimental — accuracy not yet measuredRecent studies implemented pathogenic T cells as potential diagnostic or therapeutic targets for autoimmune myocarditis including ICI myocarditis, demonstrating promising outcomes at both clinical and preclinical levels.
“Recent studies implemented pathogenic T cells as potential diagnostic or therapeutic targets for autoimmune myocarditis including ICI myocarditis, demonstrating promising outcomes at both clinical and preclinical levels. 51,64,238,254,260,311,312”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [238]
The Methods (Overview of Study Strategy) and Abstract (Results; page not provided) report Th17-cell findings in mouse myocarditis models and patients, and promising diagnostic results for a Th17-derived microRNA. The paper does not report a T-cell-targeted therapy or establish these findings specifically for immune-checkpoint-inhibitor (ICI) myocarditis. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn patient serum, myocarditis has shown an association with circulating microRNAs synthesized by Th17 cells, including mmu-miR-721 in mice and hsa-Chr8:96 in humans.
“Furthermore, in patient serum, myocarditis has shown an association with circulating microRNAs synthesized by Th17 cells, including mmu-miR-721 in mice and hsa-Chr8:96 in humans (Figure 2). 238”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [238]
The Results sections on mmu-miR-721 synthesis and detection report that Th17 cells synthesize it and that it circulates in mice with myocarditis. The Results section on hsa-miR-Chr8:96 reports its synthesis by patients’ Th17 cells and elevated levels in patients with myocarditis. The samples were plasma, however; the cited passages do not establish the claim specifically for patient serum. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn patients with myocarditis or idiopathic DCM who tested negative for specific viruses, circulating Th17 cells specific for cardiac myosin in the blood have been reported, along with a reduced number of regulatory T cells.
“In patients with myocarditis or idiopathic DCM who tested negative for specific viruses, the presence of circulating Th17 cells specific for cardiac myosin in the blood has been reported, along with a reduced number of regulatory T cells. 64,238,311”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [238]
The Results section reports increased circulating Th17 cells in patients with acute myocarditis, and the introductory passage discusses cardiac myosin-specific Th17 cells in myocarditis and dilated cardiomyopathy. The paper does not establish that these patients tested negative for specific viruses or had fewer regulatory T cells; it reports an increased Th17-to-regulatory-T-cell ratio, which does not itself show a reduced regulatory-T-cell count. (LLM, conf=0.87)
Experimental — accuracy not yet measuredHuman noncoding RNA has-Chr8:96, produced by Th17 cells, is elevated in myocarditis but not in myocardial infarction.
“A novel human noncoding RNA (has-Chr8:96), produced by Th17 cells, was recently found to be elevated in myocarditis but not in myocardial infarction”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [238]
Too many 'novel miRNAs' lack clear miRNA features and have only served to further complicate the miRNA field.
“Too many “novel miRNAs” lack clear miRNA features and have only served to further complicate the miRNA field [17, 35, 36].”
From A curated human cellular microRNAome based on 196 primary cell types (2022) · cites this paper as [36]
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- Authors
- Blanco-Domínguez, R., Sánchez-Díaz, R., de la Fuente, H., Jiménez-Borreguero, L. J., Matesanz-Marín, A., Relaño, M., Jiménez-Alejandre, R., Linillos-Pradillo, B., Tsilingiri, K., Martín-Mariscal, M. L., Alonso-Herranz, L., Moreno, G., Martín-Asenjo, R., García-Guimaraes, M. M., Bruno, K. A., Dauden, E., González-Álvaro, I., Villar-Guimerans, L. M., Martínez-León, A., Salvador-Garicano, A. M., Michelhaugh, S. A., Ibrahim, N. E., Januzzi, J. L., Kottwitz, J., Iliceto, S., Plebani, M., Basso, C., Baritussio, A., Seguso, M., Marcolongo, R., Ricote, M., Fairweather, D., Bueno, H., Fernández-Friera, L., Alfonso, F., Caforio, A. L. P., Pascual-Figal, D. A., Heidecker, B., Lüscher, T. F., Das, S., Fuster, V., Ibáñez, B., Sánchez-Madrid, F., & Martín, P.
- Affiliations
- From the Vascular Pathophysiology Area (R.B.-D., R.S.-D., A.M.-M., M. Relaño, R.J.-A., B.L.-P., K.T., D.A.P.-F., V.F., F.S.-M., P.M.) and the Myocardial Pathophysiology Area (L.A.-H., M. Ricote, H.B., L.F.-F., B.I.), Centro Nacional de Investigaciones Cardiovasculares (CNIC), the Department of Immunology (H.F., F.S.-M.), the Department of Cardiology (L.J.J.-B., M.M.G.-G., F.A.), the Department of Dermatology (E.D.), and the Department of Rheumatology (I.G.-A.), Instituto de Investigación Sanitaria, Hospital Universitario de la Princesa, Fundación Jiménez Díaz (M.L.M.-M., B.I.), the Cardiology Department, Hospital Universitario 12 de Octubre, and Instituto de Investigación Sanitaria Hospital 12 de Octubre (G.M., R.M.-A., H.B.), the Department of Immunology, Hospital Ramón y Cajal (L.M.V.-G.), HM Hospitales–Centro Integral de Enfermedades Cardiovasculares (L.F.-F.), and CIBER de Enfermedades Cardiovasculares (R.S.-D., H.F., L.J.J.-B., F.A., D.A.P.-F., B.I., F.S.-M., P.M.), Madrid, Hospital Universitario Cent...
- Research Institute Hospital 12 de Octubre (ES)
- Mayo Clinic in Florida (US)
- Harvard University (US)
- Kantonsspital St. Gallen (CH)
- Centro de Investigación Biomédica en Red (ES)
- Charité – Universitätsmedizin Berlin (DE)
- Harefield Hospital (GB)
- ORCID
- Blanco-Domínguez, Rafael
- Linillos-Pradillo, Beatriz
- Tsilingiri, Katerina
- Alonso-Herranz, Laura
- Moreno, Guillermo
- Bruno, Katelyn A.
- Michelhaugh, Sam A.
- Ibrahim, Nasrien E.
- Januzzi, James L.
- Kottwitz, Jan
- Iliceto, Sabino
- Plebani, Mario
- Basso, Cristina
- Baritussio, Anna
- Marcolongo, Renzo
- Ricote, Mercedes
- Fairweather, DeLisa
- Bueno, Héctor
- Caforio, Alida L.P.
- Pascual-Figal, Domingo A.
- Heidecker, Bettina
- Lüscher, Thomas F.
- Das, Saumya
- Ibáñez, Borja
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2021-05-27
- Volume
- 384
- Issue
- 21
- Pages
- 2014-2027
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC8258773
- OpenAlex
- W3165725306
- Cited by
- 196
- References
- 33
- Citations by year
- 2026: 32 · 2025: 29 · 2024: 33 · 2023: 41 · 2022: 45 · 2021: 16
- FWCI
- 22.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Padua Research Archive (University of Padova) (submittedVersion, other-oa)
- Funders
- American Heart Association
- Fundación BBVA
- Fundació la Marató de TV3 (20152330, 20152330 31)
- Comunidad de Madrid (S2017/BMD-3671-INFLAMUNE-CM, S2017/BMD-3671, S2017/BMD‐3867, S2017/BMD, ERC-2011-AdG 294340-GENTRIS)
- Ministerio de Economía y Competitividad (SEV‐2015‐0505, S2017/BMD-3671 -INFLAMUNE-CM, SAF2017-90604-REDT, 20152330)
- Ministerio de Ciencia e Innovación (SEV-2015-0505, RTI2018-095928-BI00, RETOS2019-107332RB-I00, S2017/BMD-3867)
- Banco Bilbao Vizcaya Argentaria
- Centro Nacional de Investigaciones Cardiovasculares (SEV‐2015‐0505)
- National Institutes of Health (UG3TR002878, TR002878)
- European Regional Development Fund (SAF2017, SEV-2015-0505, RTI2018)
- National Heart, Lung, and Blood Institute (R35HL150807)
- National Institute of Allergy and Infectious Diseases (R21AI145356, R21AI152318, R21AI154927)
- National Center for Advancing Translational Sciences
- H2020 European Research Council (819775)
- FP7 Ideas: European Research Council (294340)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- acute myocarditis, circulating microRNAs, Th17 cells, IL-17, diagnostic biomarkers, experimental autoimmune myocarditis, myocardial infarction, plasma microRNA
- MeSH terms
- Circulating MicroRNA, Animals, Autoimmune Diseases, Diagnosis, Differential, Disease Models, Animal, Humans, Mice, Inbred BALB C, Myocardial Infarction, Myocarditis, ROC Curve, T-Lymphocytes, Biomarkers, CD4 Antigens, Polymerase Chain Reaction, Mice, Knockout, MicroRNAs, Mice, Th17 Cells
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