Neuropilin-1 Mediates SARS-CoV-2 Infection in Bone Marrow-derived Macrophages

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Abstract

SARS-CoV-2 infection in human can cause medical complications across various tissues and organs. Despite of the advances to understanding the pathogenesis of SARS-CoV-2, its tissue tropism and interactions with host cells have not been fully understood. Existing clinical data have suggested possible SARS-CoV-2 infection in human skeleton system. In the present study, we found that authentic SARS-CoV-2 could efficiently infect human and mouse bone marrow-derived macrophages (BMMs) and alter the expression of macrophage chemotaxis and osteoclast-related genes. Importantly, in a mouse SARS-CoV-2 infection model that was enabled by the intranasal adenoviral (AdV) delivery of human angiotensin converting enzyme 2 (hACE2), SARS-CoV-2 was found to be present in femoral BMMs as determined by in situ immunofluorescence analysis. Using single-cell RNA sequencing (scRNA-Seq), we characterized SARS-CoV-2 infection in BMMs. Importantly, SARS-CoV-2 entry on BMMs appeared to be dependent on the expression of neuropilin-1 (NRP1) rather than the widely recognized receptor ACE2. It was also noted that unlike brain macrophages which displayed aging-dependent NRP1 expression, BMMs from neonatal and aged mice had constant NRP1 expression, making BMMs constantly vulnerable target cells for SARS-CoV-2. Furthermore, it was found that the abolished SARS-CoV-2 entry in BMM-derived osteoclasts was associated with the loss of NRP1 expression during BMM-to-osteoclast differentiation. Collectively, our study has suggested that NRP1 can mediate SARS-CoV-2 infection in BMMs, which precautions the potential impact of SARS-CoV-2 infection on human skeleton system.

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  1. SciScore for 10.1101/2021.04.14.439793: (What is this?)

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

    Table 1: Rigor

    Institutional Review Board StatementIRB: Cell culture: All experiments including human and animal tissues were approved by the ethics committee of the Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital.
    IACUC: All protocols were approved by the Institutional Animal Care and Use Committees of Guangzhou Medical University.
    Randomizationnot detected.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.
    Cell Line AuthenticationContamination: All cells were confirmed by PCR to be free of mycoplasma contamination.

    Table 2: Resources

    Antibodies
    SentencesResources
    Cells were then incubated with a rabbit anti-SARS-CoV nucleocapsid protein polyclonal antibody (Cat. No.: 40143-T62, Sino Biological, Inc. Beijing), followed by an HRP-labelled goat anti-rabbit secondary antibody (Cat. No.: 111-035-144, Jackson ImmunoResearch Laboratories, Inc. West Grove, PA).
    anti-SARS-CoV nucleocapsid protein
    suggested: (Creative Diagnostics Cat# DMAB8869, RRID:AB_2392503)
    anti-rabbit
    suggested: (Proteintech Cat# SA00006-2, RRID:AB_2651036)
    After permeabilizing in 0.1% Triton X-100 in PBS for 5 min, cells were incubated with 3% BSA-PBS for 30 min to block nonspecific antibody binding and then incubated with SARS-CoV-2 nucleocapsid protein antibody (Sino Biological), followed by incubating with Alexa Fluor 488 (Thermo).
    SARS-CoV-2 nucleocapsid protein
    suggested: (Bioss Cat# bsm-41414M, RRID:AB_2848129)
    BMMs were labelled by F4/80 antibody (Abcam), followed by incubating with Cy3-labeled Goat Anti-Rat IgG(H+L) (Beyotime).
    Anti-Rat IgG(H+L
    suggested: None
    Membranes were incubated with primary antibodies, including actin JLA20 antibody (Developmental Studies Hybridoma Bank),
    actin
    suggested: None
    Experimental Models: Cell Lines
    SentencesResources
    Vero E6 cells (derived from African Green monkey kidney) were grown in (DMEM, Thermo) supplemented with 10% FBS (Thermo) and 1% P/S (Thermo).
    Vero E6
    suggested: None
    Production and infection of SARS-CoV-2 pseudovirus: HEK293T cells were transfected with psPAX, plentiv2-Tdtomato and plasmid that carried SARS-Cov-2 S gene or empty vector using Lipofectamine 3000 (Thermo)34
    HEK293T
    suggested: None
    Experimental Models: Organisms/Strains
    SentencesResources
    SARS-CoV-2 infection in Balb/c mouse: Ad5-hACE2 transduced Balb/c mouse model were described previously25.
    Balb/c
    suggested: None
    Software and Algorithms
    SentencesResources
    Fiji (National Institutes of Health) was employed to analyze and assemble images.
    Fiji
    suggested: (Fiji, RRID:SCR_002285)
    Then the feature-barcode matrices were obtained by aligning reads to the mouse genome (GRCm38 Ensemble: version 92) using CellRanger v3.1.0
    CellRanger
    suggested: (SCIGA, RRID:SCR_021002)
    Statistical analysis: The data were graphed and statistically analysed using GraphPad Prism 8.0.
    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.