The SARS-CoV-2 Spike harbours a lipid binding pocket which modulates stability of the prefusion trimer

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Abstract

Large trimeric Spikes decorate SARS-CoV-2 and bind host cells via receptor binding domains (RBDs). We report a conformation in which the trimer is ‘locked’ into a compact well-ordered form. This differs from previous structures where the RBD can flip up to recognise the receptor. In the ‘locked’ form regions associated with fusion transitions are stabilised and the RBD harbours curved lipids. The acyl chains bind a hydrophobic pocket in one RBD whilst the polar headgroups attach to an adjacent RBD of the trimer. By functional analogy with enteroviral pocket factors loss of the lipid would destabilise the ‘locked’ form facilitating receptor attachment, conversion to the postfusion state and virus infection. The nature of lipids available at the site of infection might affect the antigenicity/pathogenicity of released virus. These results reveal a potentially druggable pocket and suggest that the natural prefusion state occludes neutralising RBD epitopes, achieving conformational shielding from antibodies.

Highlights

  • SARS-CoV-2 Spike can adopt a ‘locked’ conformation with all receptor binding domains (RBDs) down, likely to represent the prefusion resting state

  • This ‘locked’ conformation is compact and stable, braced by lipid bound within a potentially druggable pocket

  • Key neutralization epitopes are shielded in the ‘locked’ form

  • Loss of lipid may trigger a cascade of events that lead to cell entry analogous to the role of lipids in enterovirus cell entry

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  1. SciScore for 10.1101/2020.08.13.249177: (What is this?)

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

    Table 1: Rigor

    Institutional Review Board Statementnot detected.
    RandomizationThe experiments were not randomized, and investigators were not blinded to allocation during experiments and outcome assessment.
    BlindingThe experiments were not randomized, and investigators were not blinded to allocation during experiments and outcome assessment.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Experimental Models: Cell Lines
    SentencesResources
    Protein production: Recombinant Spike ectodomain was expressed by transient transfection in HEK293S GnTI-cells (ATCC CRL-3022) for 9 days at 30 °C.
    HEK293S
    suggested: ATCC Cat# CRL-3022, RRID:CVCL_A785)
    Software and Algorithms
    SentencesResources
    One good class containing around 328,000 particles was refined using non-uniform refinement to 3.3 Å and particles were exported to RELION 3.1 using pyEM
    RELION
    suggested: (RELION, RRID:SCR_016274)
    For the 3D variability analysis, polished particles and model were imported into cryoSPARC v.
    cryoSPARC
    suggested: (cryoSPARC, RRID:SCR_016501)
    Structures were modelled by first rigid body fitting the PDB ID, 6VYB (Walls et al., 2020) for the “up” conformation and by rigid body fitting individual domains for the “locked” conformation into the locally filtered map using UCSF Chimera (Pettersen et al., 2004) One cycle of rigid body real space refinement followed by manual adjustment in Coot (Emsley and Cowtan, 2004) was performed to correctly position the Cα chain into the density.
    Coot
    suggested: (Coot, RRID:SCR_014222)
    Map-to-model comparison in PHENIX (Liebschner et al., 2019) mtriage validated that no over-fitting was present in the structures.
    PHENIX
    suggested: (Phenix, RRID:SCR_014224)
    Model geometry was validated for all the refined models using MolProbity (Davis et al., 2004).
    MolProbity
    suggested: (MolProbity, RRID:SCR_014226)
    Further analysis was performed in Excel spreadsheets and Prism.
    Excel
    suggested: None
    Prism
    suggested: (PRISM, RRID:SCR_005375)

    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: 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.