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Prior flavivirus immunity skews the yellow fever vaccine response to cross-reactive antibodies with potential to enhance dengue virus infection

Author

Listed:
  • Antonio Santos-Peral

    (LMU University Hospital, LMU Munich)

  • Fabian Luppa

    (LMU University Hospital, LMU Munich)

  • Sebastian Goresch

    (LMU University Hospital, LMU Munich)

  • Elena Nikolova

    (LMU University Hospital, LMU Munich)

  • Magdalena Zaucha

    (LMU University Hospital, LMU Munich)

  • Lisa Lehmann

    (LMU University Hospital, LMU Munich)

  • Frank Dahlstroem

    (LMU University Hospital, LMU Munich)

  • Hadi Karimzadeh

    (LMU University Hospital, LMU Munich
    LMU Munich)

  • Julia Thorn-Seshold

    (LMU University Hospital, LMU Munich
    LMU Munich)

  • Elena Winheim

    (Medical Faculty, LMU Munich)

  • Ev-Marie Schuster

    (Universitätsklinikum Erlangen, Friedrich-Alexander Universität Erlangen-Nürnberg)

  • Gerhard Dobler

    (Bundeswehr Institute of Microbiology)

  • Michael Hoelscher

    (LMU University Hospital, LMU Munich
    Partner Site Munich
    Immunology, Infection and Pandemic Research)

  • Beate M. Kümmerer

    (University of Bonn
    Partner Site Bonn-Cologne)

  • Stefan Endres

    (LMU University Hospital, LMU Munich
    Einheit für Klinische Pharmakologie (EKLiP) Helmholtz Zentrum München German Research Center for Environmental Health (HMGU))

  • Kilian Schober

    (Universitätsklinikum Erlangen, Friedrich-Alexander Universität Erlangen-Nürnberg
    FAU Erlangen-Nürnberg)

  • Anne B. Krug

    (Medical Faculty, LMU Munich)

  • Michael Pritsch

    (LMU University Hospital, LMU Munich)

  • Giovanna Barba-Spaeth

    (Université Paris Cité, CNRS UMR 3569, Unité de Virologie Structurale)

  • Simon Rothenfusser

    (LMU University Hospital, LMU Munich
    Einheit für Klinische Pharmakologie (EKLiP) Helmholtz Zentrum München German Research Center for Environmental Health (HMGU))

Abstract

The yellow fever 17D vaccine (YF17D) is highly effective but is frequently administered to individuals with pre-existing cross-reactive immunity, potentially impacting their immune responses. Here, we investigate the impact of pre-existing flavivirus immunity induced by the tick-borne encephalitis virus (TBEV) vaccine on the response to YF17D vaccination in 250 individuals up to 28 days post-vaccination (pv) and 22 individuals sampled one-year pv. Our findings indicate that previous TBEV vaccination does not affect the early IgM-driven neutralizing response to YF17D. However, pre-vaccination sera enhance YF17D virus infection in vitro via antibody-dependent enhancement (ADE). Following YF17D vaccination, TBEV-pre-vaccinated individuals develop high amounts of cross-reactive IgG antibodies with poor neutralizing capacity. In contrast, TBEV-unvaccinated individuals elicit a non-cross-reacting neutralizing response. Using YF17D envelope protein mutants displaying different epitopes, we identify quaternary dimeric epitopes as the primary target of neutralizing antibodies. Additionally, TBEV-pre-vaccination skews the IgG response towards the pan-flavivirus fusion loop epitope (FLE), capable of mediating ADE of dengue and Zika virus infections in vitro. Together, we propose that YF17D vaccination conceals the FLE in individuals without prior flavivirus exposure but favors a cross-reactive IgG response in TBEV-pre-vaccinated recipients directed to the FLE with potential to enhance dengue virus infection.

Suggested Citation

  • Antonio Santos-Peral & Fabian Luppa & Sebastian Goresch & Elena Nikolova & Magdalena Zaucha & Lisa Lehmann & Frank Dahlstroem & Hadi Karimzadeh & Julia Thorn-Seshold & Elena Winheim & Ev-Marie Schuste, 2024. "Prior flavivirus immunity skews the yellow fever vaccine response to cross-reactive antibodies with potential to enhance dengue virus infection," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45806-x
    DOI: 10.1038/s41467-024-45806-x
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    References listed on IDEAS

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    1. Dennis Schaefer-Babajew & Zijun Wang & Frauke Muecksch & Alice Cho & Maximilian Loewe & Melissa Cipolla & Raphael Raspe & Brianna Johnson & Marie Canis & Justin DaSilva & Victor Ramos & Martina Turroj, 2023. "Antibody feedback regulates immune memory after SARS-CoV-2 mRNA vaccination," Nature, Nature, vol. 613(7945), pages 735-742, January.
    2. Alexander Rouvinski & Pablo Guardado-Calvo & Giovanna Barba-Spaeth & Stéphane Duquerroy & Marie-Christine Vaney & Carlos M. Kikuti & M. Erika Navarro Sanchez & Wanwisa Dejnirattisai & Wiyada Wongwiwat, 2015. "Recognition determinants of broadly neutralizing human antibodies against dengue viruses," Nature, Nature, vol. 520(7545), pages 109-113, April.
    3. Alexander Rouvinski & Wanwisa Dejnirattisai & Pablo Guardado-Calvo & Marie-Christine Vaney & Arvind Sharma & Stéphane Duquerroy & Piyada Supasa & Wiyada Wongwiwat & Ahmed Haouz & Giovanna Barba-Spaeth, 2017. "Covalently linked dengue virus envelope glycoprotein dimers reduce exposure of the immunodominant fusion loop epitope," Nature Communications, Nature, vol. 8(1), pages 1-12, August.
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