Remdesivir potently inhibits SARS-CoV-2 in human lung cells and chimeric SARS-CoV expressing the SARS-CoV-2 RNA polymerase in mice

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Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in 2019 as the causative agent of the novel pandemic viral disease COVID-19. With no approved therapies, this pandemic illustrates the urgent need for safe, broad-spectrum antiviral countermeasures against SARS-CoV-2 and future emerging CoVs. We report that remdesivir (RDV), a monophosphoramidate prodrug of an adenosine analog, potently inhibits SARS-CoV-2 replication in human lung cells and primary human airway epithelial cultures (EC 50 = 0.01 μM). Weaker activity was observed in Vero E6 cells (EC 50 = 1.65 μM) due to their low capacity to metabolize RDV. To rapidly evaluate in vivo efficacy, we engineered a chimeric SARS-CoV encoding the viral target of RDV, the RNA-dependent RNA polymerase, of SARS-CoV-2. In mice infected with chimeric virus, therapeutic RDV administration diminished lung viral load and improved pulmonary function as compared to vehicle treated animals. These data provide evidence that RDV is potently active against SARS-CoV-2 in vitro and in vivo , supporting its further clinical testing for treatment of COVID-19.

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  1. SciScore for 10.1101/2020.04.27.064279: (What is this?)

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

    Table 1: Rigor

    Institutional Review Board StatementIRB: Human tracheobronchial epithelial cells provided by Dr. Scott Randell were obtained from airway specimens resected from patients undergoing surgery under University of North Carolina Institutional Review Board-approved protocols (#03-1396) by the Cystic Fibrosis Center Tissue Culture Core.
    IACUC: In vivo efficacy studies: All animal experiments were performed in accordance with the University of North Carolina at Chapel Hill Institutional Animal Care and Use Committee policies and guidelines.
    Randomizationnot detected.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variableThe HAE donors were 56- and 62-year-old females of the same race.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Experimental Models: Cell Lines
    SentencesResources
    Cells, viruses, and compounds: Vero (ATCC CCL-81) and Vero E6 (ATCC CRL-1586) cells were purchased from ATCC and cultured in DMEM supplemented with 10% fetal bovine serum (FBS) (Gibco, ThermoFisher Scientific) or 10% FCS fetal clonal serum (FCS)(HyClone, GE Life Sciences), 100 U/ml penicillin and streptomycin (Gibco, ThermoFisher Scientific), and 0.25 μM amphotericin B (
    Vero
    suggested: ATCC Cat# CRL-1586, RRID:CVCL_0574)
    Antiviral activity assays: Vero E6 cells were seeded at 1 x 105 cells per well, and Calu3 2B4 cells were seeded at 2 x 105 cells per well in 24-well plates (Corning).
    Calu3 2B4
    suggested: RRID:CVCL_YZ47)
    Huh7 cells were plated at a density of 8 x 104 cells per well.
    Huh7
    suggested: None
    Cytotoxicity Assays: Cells were seeded at a density of 15,000 cells/well (Vero E6) or 30,000 cells/well
    Vero E6
    suggested: RRID:CVCL_XD71)
    Experimental Models: Organisms/Strains
    SentencesResources
    To achieve a pharmacokinetic profile similar to that observed in humans, we performed therapeutic efficacy studies in Ces1-/- mice (stock 014096, The Jackson Laboratory), which lack a serum esterase not present in humans that dramatically reduces RDV half-life (Sheahan et al., 2017).
    Ces1-/-
    suggested: None
    Software and Algorithms
    SentencesResources
    All statistical tests were executed using GraphPad Prism 8.
    GraphPad Prism
    suggested: (GraphPad Prism, RRID:SCR_002798)

    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: No clinical trial numbers were referenced.


    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.

  2. SciScore for 10.1101/2020.04.27.064279: (What is this?)

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

    Table 1: Rigor

    Institutional Review Board StatementHuman tracheobronchial epithelial cells provided by Dr. Scott Randell were obtained from airway specimens resected from patients undergoing surgery under University of North Carolina Institutional Review Board-approved protocols ( #03-1396 ) by the Cystic Fibrosis Center Tissue Culture Core.RandomizationPrior to the emergence of pandemic SARS-CoV-2 , RDV was evaluated in phase 1 clinical trials as well as phase 2 randomized controlled trial trials to treat acute Ebola virus disease in the Democratic Republic of Congo ( DRC) , and human safety data are available ( Mulangu et al. , 2019) .Blindingnot detected.Power Analysisnot detected.Sex as a biological variableWe infected female C57Bl/6 Ces1c-/- mice with 103 PFU SARS1/SARS2-RdRp and initiated subcutaneous treatment with 25 mg/kg 6 RDV BID at one day post-infection ( dpi) .Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    Broad-spectrum antiviral drugs , antibodies , and vaccines are needed to combat the current pandemic and those that will emerge in the future.
    antiviral drugs ,
    suggested: None
    Therapies combining direct-acting antivirals ( DAAs ) such as RDV and NHC , along with other DAAs such as antibodies and protease inhibitors that target different stages of the viral replication cycle , could be considered for counteracting resistance if it emerges in patients treated with antiviral monotherapy .
    antiviral monotherapy .
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    To determine if RDV and GS-441524 inhibit SARS-CoV-2 replication in established cell lines , Calu3 2B4 human lung adenocarcinoma cells and Vero E6 African green monkey kidney cells were infected with the SARS-CoV-2 clinical isolate 2019-nCoV/USA-WA1/2020 and treated with a range of RDV or GS-441524 concentrations .
    Vero E6
    suggested: None
    In addition , SARS-CoV-1 infects Huh7 cells at low frequency at the MOI used in this study and does not appear to spread throughout the culture over the course of the experiment .
    Huh7
    suggested: CLS Cat# 300156/p7178_HuH7, CVCL_0336
    Calu3 cells were infected with 0.1 PFU/cell SARS-CoV-2 and Vero cells were infected with 0.01 PFU/cell SARS-CoV-2 and treated with RDV , GS-441524 ( ‘524) , or DMSO only ( control ) in cell culture medium .
    Calu3
    suggested: BCRJ Cat# 0264, CVCL_0609
          <div style="margin-bottom:8px">
            <div><b>Vero</b></div>
            <div>suggested: None</div>
          </div>
        </td></tr><tr><td style="min-width:100px;vertical-align:top;border-bottom:1px solid lightgray">Vero E6 cells were seeded at 1 x 105 cells per well , and Calu3 2B4 cells were seeded at 2 x 105 cells per well in 24-well plates ( Corning) .</td><td style="min-width:100px;border-bottom:1px solid lightgray">
          <div style="margin-bottom:8px">
            <div><b>Calu3 2B4</b></div>
            <div>suggested: None</div>
          </div>
        </td></tr></table>
    

    Results from Barzooka: We also found bar graphs of continuous data. We recommend replacing bar graphs with more informative graphics, as many different datasets can lead to the same bar graph. The actual data may suggest different conclusions from the summary statistics. For more information, please see Weissgerber et al (2015).

    Results from OddPub: Thank you for sharing your data.


    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 is not a substitute for expert review. SciScore checks for the presence and correctness of RRIDs (research resource identifiers) in the manuscript, and detects sentences that appear to be missing RRIDs. SciScore also checks to make sure that rigor criteria are addressed by authors. It does this by detecting sentences that discuss criteria such as blinding or power analysis. SciScore does not guarantee that the rigor criteria that it detects are appropriate for the particular study. Instead it assists authors, editors, and reviewers by drawing attention to sections of the manuscript that contain or should contain various rigor criteria and key resources. For details on the results shown here, please follow this link.