A monocyte/dendritic cell molecular signature of SARS-CoV-2-related multisystem inflammatory syndrome in children with severe myocarditis

Med. 2021 Sep 10;2(9):1072-1092.e7. doi: 10.1016/j.medj.2021.08.002. Epub 2021 Aug 14.

Abstract

Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in children is generally milder than in adults, but a proportion of cases result in hyperinflammatory conditions often including myocarditis.

Methods: To better understand these cases, we applied a multiparametric approach to the study of blood cells of 56 children hospitalized with suspicion of SARS-CoV-2 infection. Plasma cytokine and chemokine levels and blood cellular composition were measured, alongside gene expression at the bulk and single-cell levels.

Findings: The most severe forms of multisystem inflammatory syndrome in children (MIS-C) related to SARS-CoV-2 that resulted in myocarditis were characterized by elevated levels of pro-angiogenesis cytokines and several chemokines. Single-cell transcriptomics analyses identified a unique monocyte/dendritic cell gene signature that correlated with the occurrence of severe myocarditis characterized by sustained nuclear factor κB (NF-κB) activity and tumor necrosis factor alpha (TNF-α) signaling and associated with decreased gene expression of NF-κB inhibitors. We also found a weak response to type I and type II interferons, hyperinflammation, and response to oxidative stress related to increased HIF-1α and Vascular endothelial growth factor (VEGF) signaling.

Conclusions: These results provide potential for a better understanding of disease pathophysiology.

Funding: Agence National de la Recherche (Institut Hospitalo-Universitaire Imagine, grant ANR-10-IAHU-01; Recherche Hospitalo-Universitaire, grant ANR-18-RHUS-0010; Laboratoire d'Excellence ''Milieu Intérieur," grant ANR-10-LABX-69-01; ANR-flash Covid19 "AIROCovid" and "CoVarImm"), Institut National de la Santé et de la Recherche Médicale (INSERM), and the "URGENCE COVID-19" fundraising campaign of Institut Pasteur.

Keywords: COVID-19; Kawasaki Disease; MIS-C; PIMS-TS; SARS-CoV-2; TNF-α and NF-κB signaling; lack of responses to type I and type II IFN secretion; myocarditis; scRNA-seq.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • COVID-19* / complications
  • Chemokines
  • Child
  • Cytokines
  • Dendritic Cells
  • Humans
  • Monocytes
  • Myocarditis*
  • NF-kappa B
  • SARS-CoV-2 / genetics
  • Systemic Inflammatory Response Syndrome
  • Vascular Endothelial Growth Factor A

Substances

  • Chemokines
  • Cytokines
  • NF-kappa B
  • Vascular Endothelial Growth Factor A

Supplementary concepts

  • pediatric multisystem inflammatory disease, COVID-19 related