Coagulation factors directly cleave SARS-CoV-2 spike and enhance viral entry

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Abstract

Coagulopathy is a significant aspect of morbidity in COVID-19 patients. The clotting cascade is propagated by a series of proteases, including factor Xa and thrombin. While certain host proteases, including TMPRSS2 and furin, are known to be important for cleavage activation of SARS-CoV-2 spike to promote viral entry in the respiratory tract, other proteases may also contribute. Using biochemical and cell-based assays, we demonstrate that factor Xa and thrombin can also directly cleave SARS-CoV-2 spike, enhancing infection at the stage of viral entry. Coagulation factors increased SARS-CoV-2 infection in human lung organoids. A drug-repurposing screen identified a subset of protease inhibitors that promiscuously inhibited spike cleavage by both transmembrane serine proteases and coagulation factors. The mechanism of the protease inhibitors nafamostat and camostat may extend beyond inhibition of TMPRSS2 to coagulation-induced spike cleavage. Anticoagulation is critical in the management of COVID-19, and early intervention could provide collateral benefit by suppressing SARS-CoV-2 viral entry. We propose a model of positive feedback whereby infection-induced hypercoagulation exacerbates SARS-CoV-2 infectivity.

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  1. SciScore for 10.1101/2021.03.31.437960: (What is this?)

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

    Table 1: Rigor

    Institutional Review Board Statementnot detected.
    Randomizationnot detected.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.
    Cell Line AuthenticationContamination: Cell Culture: Calu3, A549, Caco2, and Vero cells were tested for mycoplasma (Lonza MycoAlert detection kit) and human cell line identity was authenticated by ATCC.

    Table 2: Resources

    Antibodies
    SentencesResources
    Prior to infection of target cells, the viral stock was incubated with anti-VSV-G antibody (3ug/ml) for 1 h at 37°C to neutralize contaminating rVSVΔG/NG/NanoLuc/VSV-G particles.
    anti-VSV-G
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    Cell Culture: Calu3, A549, Caco2, and Vero cells were tested for mycoplasma (Lonza MycoAlert detection kit) and human cell line identity was authenticated by ATCC.
    Vero
    suggested: CLS Cat# 605372/p622_VERO, RRID:CVCL_0059)
    A549 and Vero cells were grown in DMEM, supplemented with 10% FBS, 100U/ml Penicillin, and 100ug/ml Streptomycin.
    A549
    suggested: None
    Calu3 and Caco2 cells were grown in MEM, supplemented with 10% FBS, 100U/ml Penicillin, 100ug/ml Streptomycin, 1% MEM NEAA and 1mM sodium pyruvate.
    Caco2
    suggested: None
    Lentiviral vectors were co-transduced with MD2G and PAX2 in 293T cells (5 million cells/10cm plate) with 25ul of XtremeGene9 (Millipore Sigma, #6365787001) and supernatant was harvested at 48hr and 72hr post transfection.
    293T
    suggested: None
    Software and Algorithms
    SentencesResources
    Calculation of enzyme constants was performed with Graphpad Prism software (version 9.0).
    Graphpad Prism
    suggested: (GraphPad Prism, RRID:SCR_002798)
    GFP+RFP+ cells were quantified using a BD Attune NxT Flow cytometer (Thermo Fisher Scientific) and data was analyzed in FlowJo version 10.7.1.
    FlowJo
    suggested: (FlowJo, RRID:SCR_008520)

    Results from OddPub: We did not detect open data. We also did not detect open code. Researchers are encouraged to share open data when possible (see Nature blog).


    Results from LimitationRecognizer: We detected the following sentences addressing limitations in the study:
    Limitations: The experiments of this study, like prior studies using similar techniques, have some limitations. Protease enzymatic assays on peptide substrates allow for detailed biochemical characterization of a specific site, but peptide substrates may not have the equivalent three-dimensional conformation or post-translational modifications of the full-length protein produced in appropriate cells. For instance, SARS-CoV-2 S is extensively glycosylated (Watanabe et al., 2020). Pseudovirus and syncytia formation provide complementary functional assays, dependent on homotrimeric spike protein produced in human cells. The possibility of additional spike cleavage sites and potential pro- and anti-viral consequence of proteases acting on cell surface proteins including ACE2 cannot be excluded. The amount, density, and accessibility of spike protein could be different between these cell-based surrogate assays and wild type SARS-CoV-2 infection. However, antibody neutralization is highly correlated between authentic virus and corresponding pseudotyped viruses, suggesting similar conformation (Schmidt et al., 2020). We have mitigated the risk of artifact by using multiple orthogonal platforms, including VSV-based pseudovirus, HIV-based pseudovirus, and syncytia formation.

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

    IdentifierStatusTitle
    NCT02735707RecruitingRandomized, Embedded, Multifactorial Adaptive Platform Trial…
    NCT04505774RecruitingAnti-thrombotics for Adults Hospitalized With COVID-19 (ACTI…
    NCT04372589Active, not recruitingAntithrombotic Therapy to Ameliorate Complications of COVID-…


    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.

    About SciScore

    SciScore is an automated tool that is designed to assist expert reviewers by finding and presenting formulaic information scattered throughout a paper in a standard, easy to digest format. SciScore checks for the presence and correctness of RRIDs (research resource identifiers), and for rigor criteria such as sex and investigator blinding. For details on the theoretical underpinning of rigor criteria and the tools shown here, including references cited, please follow this link.