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EBioMedicine . Endothelial thrombomodulin downregulation caused by hypoxia contributes to severe infiltration and coagulopathy in COVID-19 patient

tetano

Editor, Senior Moderator
EBioMedicine


. 2022 Jan 13;75:103812.
doi: 10.1016/j.ebiom.2022.103812. Online ahead of print.
Endothelial thrombomodulin downregulation caused by hypoxia contributes to severe infiltration and coagulopathy in COVID-19 patient lungs


Taejoon Won[SUP] 1 [/SUP], Megan K Wood[SUP] 2 [/SUP], David M Hughes[SUP] 3 [/SUP], Monica V Talor[SUP] 1 [/SUP], Zexu Ma[SUP] 2 [/SUP], Jowaly Schneider[SUP] 1 [/SUP], John T Skinner[SUP] 4 [/SUP], Beejan Asady[SUP] 2 [/SUP], Erin Goerlich[SUP] 5 [/SUP], Marc K Halushka[SUP] 1 [/SUP], Allison G Hays[SUP] 5 [/SUP], Deok-Ho Kim[SUP] 6 [/SUP], Chirag R Parikh[SUP] 7 [/SUP], Avi Z Rosenberg[SUP] 1 [/SUP], Isabelle Coppens[SUP] 2 [/SUP], Roger A Johns[SUP] 4 [/SUP], Nisha A Gilotra[SUP] 5 [/SUP], Jody E Hooper[SUP] 1 [/SUP], Andrew Pekosz[SUP] 2 [/SUP], Daniela Čiháková[SUP] 8 [/SUP]



Affiliations

Abstract

Background: Thromboembolism is a life-threatening manifestation of coronavirus disease 2019 (COVID-19). We investigated a dysfunctional phenotype of vascular endothelial cells in the lungs during COVID-19.
Methods: We obtained the lung specimens from the patients who died of COVID-19. The phenotype of endothelial cells and immune cells was examined by flow cytometry and immunohistochemistry (IHC) analysis. We tested the presence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in the endothelium using IHC and electron microscopy.
Findings: The autopsy lungs of COVID-19 patients exhibited severe coagulation abnormalities, immune cell infiltration, and platelet activation. Pulmonary endothelial cells of COVID-19 patients showed increased expression of procoagulant von Willebrand factor (VWF) and decreased expression of anticoagulants thrombomodulin and endothelial protein C receptor (EPCR). In the autopsy lungs of COVID-19 patients, the number of macrophages, monocytes, and T cells was increased, showing an activated phenotype. Despite increased immune cells, adhesion molecules such as ICAM-1, VCAM-1, E-selectin, and P-selectin were downregulated in pulmonary endothelial cells of COVID-19 patients. Notably, decreased thrombomodulin expression in endothelial cells was associated with increased immune cell infiltration in the COVID-19 patient lungs. There were no SARS-CoV-2 particles detected in the lung endothelium of COVID-19 patients despite their dysfunctional phenotype. Meanwhile, the autopsy lungs of COVID-19 patients showed SARS-CoV-2 virions in damaged alveolar epithelium and evidence of hypoxic injury.
Interpretation: Pulmonary endothelial cells become dysfunctional during COVID-19, showing a loss of thrombomodulin expression related to severe thrombosis and infiltration, and endothelial cell dysfunction might be caused by a pathologic condition in COVID-19 patient lungs rather than a direct infection with SARS-CoV-2.
Funding: This work was supported by the Johns Hopkins University, the American Heart Association, and the National Institutes of Health.

Keywords: COVID-19; SARS-CoV-2; endothelial cell dysfunction; immunothrombosis;
 
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