A spike-ferritin nanoparticle vaccine induces robust innate immune activity and drives polyfunctional SARS-CoV-2-specific T cells

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Abstract

Potent cellular responses to viral infections are pivotal for long -lived protection. Evidence is growing that these responses are critical in SARS -CoV-2 immunity. Assessment of a SARS -CoV-2 spike ferritin nanoparticle (SpFN) immunogen paired with two distinct adjuvants, Alhydrogel® (AH) or Army Liposome Formulation containing QS-21 (ALFQ) demonstrated unique vaccine evoked immune signatures. SpFN+ALFQ enhanced recruitment of highly activated classical and non -classical antigen presenting cells (APCs) to the vaccine-draining lymph nodes of mice. The multifaceted APC response of SpFN+ALFQ vaccinated mice was associated with an increased frequency of polyfunctional spike -specific T cells with a bias towards T H 1 responses and more robust SARS-CoV-2 spike-specific recall response. In addition, SpFN+ALFQ induced K b spike (539-546) -specific memory CD8 + T cells with effective cytolytic function and distribution to the lungs. This epitope is also present in SARS-CoV, thus suggesting that generation of cross-reactive T cells may provide protection against other coronavirus strains. Our study reveals that a nanoparticle vaccine, combined with a potent adjuvant, generates effective SARS-CoV-2 specific innate and adaptive immune T cell responses that are key components to inducing long-lived immunity.

One Sentence Summary

SpFN vaccine generates multifactorial cellular immune responses.

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  1. SciScore for 10.1101/2021.04.28.441763: (What is this?)

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

    Table 1: Rigor

    EthicsIACUC: The protocols were approved by the Institutional Animal Care and Use Committee at the Walter Reed Army Institute of Research [Assurance number D16-00596 (A4117-01)].
    Sex as a biological variableMice vaccination and tissue processing: Female C57BL/6 mice (5-6 weeks of age) were obtained from The Jackson Laboratory.
    RandomizationMice were age- and sex-matched and were randomly assigned to study groups.
    BlindingThe APC flow cytometry and ELISpot analysis were performed by the investigators in a blinded fashion as they were not aware of which treatment group belonged to which adjuvant formulation.
    Power Analysisnot detected.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    After the incubation period, cells were stained with LIVE/DEAD Fixable Aqua Dead Cell Stain Kit (Invitrogen), followed by surface staining with antibodies specific for the following cell surface markers (BUV737 anti -CD3, BUV395 anti-CD4, BV711 anti-CD8 (table S4), obtained from either BD Biosciences, Thermo Fisher Scientific or Biolegend, washed twice with FACS buffer and then fixed/permeabilized for 40 mins at 4°C in the dark using the eBioscience™ Intracellular Fixation & Permeabilization Buffer Set (Thermo Fisher Scientific) as per the manufacturer’s instructions.
    anti -CD3, BUV395
    suggested: (BD Biosciences Cat# 563878, RRID:AB_2631259)
    anti-CD4
    suggested: None
    BV711
    suggested: None
    anti-CD8
    suggested: None
    Cells were then incubated with a panel of intracellular antibodies specific for the following cytokines (V450 anti -IFN-γ, FITC anti-TNF-α, PerCP-Cy5 anti-IL-4, PE anti IL-2; table S4) for 30 min at 4°C, washed twice, and resuspended in FACS buffer.
    anti -IFN-γ, FITC
    suggested: None
    anti-IL-4
    suggested: None
    anti IL-2; table S4
    suggested: None
    ELISpot: Multiscreen plates (Millipore, Bedford MA) were coated with anti-IFN-γ antibody (capture mAb; 1 µg/mL) according to the manufacturer’s instructions (R&D Systems, Minneapolis, MN).
    anti-IFN-γ
    suggested: None
    Plates were incubated with biotinylated anti -IFN-γ antibody (detecting mAb; 1 µg/mL) overnight at 4°C.
    anti -IFN-γ
    suggested: None
    In the last 20 min of tetramer incubation, the following mix of fluorescent antibodies were added: BUV737-anti-mouse CD3, BUV395-anti-mouse CD4, BV711-anti-mouse CD8a and antibodies directed towards intracellular cytokines such as V450 anti -IFN-γ, FITC anti-TNF-α, and APC anti IL-2 (Supplementary Table 4), then washed twice and resuspended in FACS buffer.
    CD3
    suggested: None
    BUV395-anti-mouse CD4
    suggested: None
    BV711-anti-mouse
    suggested: None
    CD8a
    suggested: (BD Biosciences Cat# 560471, RRID:AB_1645282)
    Experimental Models: Cell Lines
    SentencesResources
    The protein was transiently expressed as a soluble recombinant protein in mammalian Expi293 cells (Thermo Fisher Scientific).
    Expi293
    suggested: RRID:CVCL_D615)
    Experimental Models: Organisms/Strains
    SentencesResources
    Mice vaccination and tissue processing: Female C57BL/6 mice (5-6 weeks of age) were obtained from The Jackson Laboratory.
    C57BL/6
    suggested: None
    Software and Algorithms
    SentencesResources
    For vaccine preparations adjuvanted with ALFQ, SpFN (600 µg/mL) was mixed with ALFQ (1.5X) in a 1:2 volume ratio.
    ALFQ
    suggested: (aLFQ, RRID:SCR_005925)
    Evaluation of co-expression of different cytokines was performed using the FlowJo Boolean gate platform.
    FlowJo
    suggested: (FlowJo, RRID:SCR_008520)
    CFSE high and low solutions were made at 0.5 and 0.05 µM respectively using ThermoFisher CellTrace™ CFSE Cell Proliferation Kit (Catalog C34554).
    ThermoFisher CellTrace™
    suggested: None
    Statistical analyses were conducted using GraphPad Prism v.8.4.0 software.
    GraphPad Prism
    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
    NCT03186781CompletedInfluenza HA Ferritin Vaccine, Alone or in Prime-Boost Regim…
    NCT03814720CompletedDose, Safety, Tolerability and Immunogenicity of an Influenz…
    NCT04645147RecruitingSafety and Immunogenicity of an Epstein-Barr Virus (EBV) gp3…
    NCT04579250RecruitingDose, Safety, Tolerability and Immunogenicity of an Influenz…
    NCT04784767RecruitingSARS-COV-2-Spike-Ferritin-Nanoparticle (SpFN) Vaccine With A…


    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 page 45. 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.
    • Thank you for including a protocol registration statement.

    Results from scite Reference Check: We found no unreliable references.


    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.