Topical TMPRSS2 inhibition prevents SARS-CoV-2 infection in differentiated primary human airway cells

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Abstract

Background

There are limited effective prophylactic treatments for SARS-CoV-2 infection, and limited early treatment options. Viral cell entry requires spike protein binding to the ACE2 receptor and spike cleavage by TMPRSS2, a cell surface serine protease. Targeting of TMPRSS2 by either androgen blockade or direct inhibition is already in clinical trials in early SARS-CoV-2 infection.

Methods

The likely initial cells of SARS-CoV-2 entry are the ciliated cells of the upper airway. We therefore used differentiated primary human airway epithelial cells maintained at the air-liquid interface (ALI) to test the impact of targeting TMPRSS2 on the prevention of SARS-CoV-2 infection.

Results

We first modelled the systemic delivery of compounds. Enzalutamide, an oral androgen receptor antagonist, had no impact on SARS-Cov-2 infection. By contrast, camostat mesylate, an orally available serine protease inhibitor, blocked SARS-CoV-2 entry. However, camostat is rapidly metabolised in the circulation in vivo , and systemic bioavailability after oral dosing is low. We therefore modelled local airway administration by applying camostat to the apical surface of the differentiated ALI cultures. We demonstrated that a brief exposure to topical camostat is effective at restricting SARS-CoV-2 viral infection.

Conclusion

These experiments demonstrate a potential therapeutic role for topical camostat for pre- or post-exposure prophylaxis of SARS-CoV-2, which can now be evaluated in a clinical trial.

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  1. SciScore for 10.1101/2021.04.23.440619: (What is this?)

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

    Table 1: Rigor

    EthicsIRB: model: Human airway epithelial cells (hAECs) were purchased from Lonza or were expanded directly from either bronchial brushings from a main airway at bronchoscopy or a nasal brushing from the inferior turbinate from patients at Cambridge University Hospitals NHS Trust (Research Ethics Committee Reference 19/SW/0152).
    Sex as a biological variableSpecific cells used were human bronchial epithelial cells (HBECs) derived from a non-smoking donor (Lonza; Cat# CC-2540, male); human bronchial epithelial cells from a male smoking donor undergoing bronchoscopy for a non-cancer indication, and nasal epithelial cells (MOD006) from a male patient.
    Randomizationnot detected.
    Blindingnot detected.
    Power Analysisnot detected.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    Permeabilised cells were pelleted, stained for 15 minutes at room temperature in 100 μL of sheep anti-SARS-CoV-2 nucleoprotein antibody (MRC-PPU, DA114) at a concentration of 0.7 μg/mL, washed and incubated in 100 μL AF488 donkey anti-sheep (Jackson ImmunoResearch #713-545-147) at a concentration of 2 μg/mL for 15 minutes at room temperature.
    anti-SARS-CoV-2 nucleoprotein
    suggested: None
    anti-sheep
    suggested: (Jackson ImmunoResearch Labs Cat# 713-545-147, RRID:AB_2340745)
    The following antibodies were used: Anti-ACE2 antibody (Anti-ACE2 antibody - N-terminal, ab228349 was originally used.
    Anti-ACE2
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    Viral titre was determined by 50% tissue culture infectious dose (TCID50) in Huh7-ACE2 cells.
    Huh7-ACE2
    suggested: None
    Software and Algorithms
    SentencesResources
    % Cytotoxicity was calculated:

    Quantification and statistical analysis: Statistical analyses of mRNA expression assays and infection quantification data were performed using Prism 8 software (GraphPad Software).

    Prism
    suggested: (PRISM, RRID:SCR_005375)
    GraphPad
    suggested: (GraphPad Prism, RRID:SCR_002798)

    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: 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
    NCT04446429CompletedAnti-Androgen Treatment for COVID-19
    NCT04475601RecruitingEnzalutamide Treatment in COVID-19
    NCT04455815RecruitingA Trial Looking at the Use of Camostat to Reduce Progression…
    NCT04608266RecruitingCAMOVID : Evaluation of Efficacy and Safety of Camostat Mesy…


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


    Results from JetFighter: Please consider improving the rainbow (“jet”) colormap(s) used on pages 32, 29, 30 and 31. At least one figure is not accessible to readers with colorblindness and/or is not true to the data, i.e. not perceptually uniform.


    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.