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

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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 Factor XIII (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, plasma FXII 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 NETs/FXII axis contributes to the pathogenic chain of procoagulant and proinflammatory responses in COVID-19. Targeting both, NETs and FXIIa, could provide a strategy to mitigate COVID-19-induced thrombo-inflammation.

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).

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  1. SciScore for 10.1101/2020.12.29.424644: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    Institutional Review Board StatementIRB: Acquisition of patient plasma samples: Heparinized plasma samples were obtained from SARS-CoV-2 positive patients hospitalized at the University Medical Center Hamburg, Germany during the first outbreak in April 2020 (permit number #2322, Ethics Committee of the Hamburg Medical Association, Hamburg, Germany).
    RandomizationThe experiments were not randomized.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    The following antibodies were used: anti-neutrophil elastase (5 μg/ml, ab121595, Abcam)
    anti-neutrophil elastase ( 5
    suggested: None
    Software and Algorithms
    SentencesResources
    The diameter of DNase digestion was measured using Image J.
    Image J
    suggested: (ImageJ, RRID:SCR_003070)
    Statistics: GraphPad Prism was used for graphic representation and statistical analysis of data.
    GraphPad
    suggested: (GraphPad Prism, RRID:SCR_002798)
    The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium22 via the PRIDE23 partner repository with the dataset identifier PXD020216.
    ProteomeXchange
    suggested: (ProteomeXchange, RRID:SCR_004055)

    Results from OddPub: Thank you for sharing your data.


    Results from LimitationRecognizer: An explicit section about the limitations of the techniques employed in this study was not found. We encourage authors to address study limitations.

    Results from TrialIdentifier: We found the following clinical trial numbers in your paper:

    IdentifierStatusTitle
    NCT04355364RecruitingEfficacy and Safety of aerosolizedDornase Alfa Administratio…
    NCT04402970CompletedDornase Alfa for ARDS in Patients With SARS-CoV-2
    NCT04445285RecruitingPhase 2 Trial Using rhDNase to Reduce Mortality in COVID-19 …
    NCT04432987RecruitingDornase Alpha for the Treatment of COVID-19
    NCT04359654RecruitingNebulised Dornase Alfa for Treatment of COVID-19
    NCT04402944RecruitingPulmozyme to Improve COVID-19 ARDS Outcomes
    NCT04524962RecruitingStudy of Descartes-30 in Acute Respiratory Distress Syndrome
    NCT04541979RecruitingAerosoliserat DNase for Treatment of Respiratory Failure in …
    NCT04409925RecruitingDISmantling COvid iNduced Neutrophil ExtraCellular Traps (DI…
    NCT04409509CompletedTreatment With CSL312 in Adults With Coronavirus Disease 201…


    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.


    Results from JetFighter: We did not find any issues relating to colormaps.


    Results from rtransparent:
    • Thank you for including a conflict of interest statement. Authors are encouraged to include this statement when submitting to a journal.
    • Thank you for including a funding statement. Authors are encouraged to include this statement when submitting to a journal.
    • No protocol registration statement was detected.

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