Defective NET clearance contributes to sustained FXII activation in COVID-19-associated pulmonary thrombo-inflammation

EBioMedicine. 2021 May:67:103382. doi: 10.1016/j.ebiom.2021.103382. Epub 2021 May 14.

Abstract

Background: Coagulopathy and inflammation are hallmarks of Coronavirus disease 2019 (COVID-19) and are associated with increased mortality. Clinical and experimental data have revealed a role for neutrophil extracellular traps (NETs) in COVID-19 disease. The mechanisms that drive thrombo-inflammation in COVID-19 are poorly understood.

Methods: We performed proteomic analysis and immunostaining of postmortem lung tissues from COVID-19 patients and patients with other lung pathologies. We further compared coagulation factor XII (FXII) and DNase activities in plasma samples from COVID-19 patients and healthy control donors and determined NET-induced FXII activation using a chromogenic substrate assay.

Findings: FXII expression and activity were increased in the lung parenchyma, within the pulmonary vasculature and in fibrin-rich alveolar spaces of postmortem lung tissues from COVID-19 patients. In agreement with this, plasmaaac acafajföeFXII activation (FXIIa) was increased in samples from COVID-19 patients. Furthermore, FXIIa colocalized with NETs in COVID-19 lung tissue indicating that NETs accumulation leads to FXII contact activation in COVID-19. We further showed that an accumulation of NETs is partially due to impaired NET clearance by extracellular DNases as DNase substitution improved NET dissolution and reduced FXII activation in vitro.

Interpretation: Collectively, our study supports that the NET/FXII axis contributes to the pathogenic chain of procoagulant and proinflammatory responses in COVID-19. Targeting both NETs and FXIIa may offer a potential novel therapeutic strategy.

Funding: This study was supported by the European Union (840189), the Werner Otto Medical Foundation Hamburg (8/95) and the German Research Foundation (FR4239/1-1, A11/SFB877, B08/SFB841 and P06/KFO306).

Keywords: COVID-19; FXII; NETs; Pulmonary thrombo-inflammation; Thrombosis.

MeSH terms

  • Autopsy
  • COVID-19 / metabolism*
  • Case-Control Studies
  • Deoxyribonucleases / blood
  • Deoxyribonucleases / metabolism
  • Extracellular Traps / metabolism*
  • Factor XII / metabolism*
  • Humans
  • Lung / metabolism
  • Neutrophil Activation
  • Pneumonia
  • Proteomics

Substances

  • Factor XII
  • Deoxyribonucleases