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Omicron infection following vaccination enhances a broad spectrum of immune responses dependent on infection history

Author

Listed:
  • Hailey Hornsby

    (The University of Sheffield)

  • Alexander R. Nicols

    (Newcastle University)

  • Stephanie Longet

    (University of Oxford
    University of Oxford)

  • Chang Liu

    (University of Oxford)

  • Adriana Tomic

    (Boston University
    Boston University School of Medicine
    Boston University
    University of Oxford)

  • Adrienn Angyal

    (The University of Sheffield)

  • Barbara Kronsteiner

    (University of Oxford
    University of Oxford)

  • Jessica K. Tyerman

    (Newcastle University)

  • Tom Tipton

    (University of Oxford
    University of Oxford)

  • Peijun Zhang

    (The University of Sheffield)

  • Marta Gallis

    (The University of Sheffield)

  • Piyada Supasa

    (University of Oxford)

  • Muneeswaran Selvaraj

    (University of Oxford)

  • Priyanka Abraham

    (University of Oxford
    University of Oxford)

  • Isabel Neale

    (University of Oxford
    University of Oxford)

  • Mohammad Ali

    (University of Oxford
    University of Oxford)

  • Natalie A. Barratt

    (The University of Sheffield)

  • Jeremy M. Nell

    (Newcastle University
    Newcastle upon Tyne Hospitals NHS Foundation Trust)

  • Lotta Gustafsson

    (The University of Sheffield
    Sheffield Teaching Hospitals NHS Foundation Trust)

  • Scarlett Strickland

    (The University of Sheffield
    Sheffield Teaching Hospitals NHS Foundation Trust)

  • Irina Grouneva

    (The University of Sheffield)

  • Timothy Rostron

    (University of Oxford)

  • Shona C. Moore

    (University of Liverpool)

  • Luisa M. Hering

    (University of Liverpool)

  • Susan L. Dobson

    (University of Liverpool)

  • Sagida Bibi

    (University of Oxford)

  • Juthathip Mongkolsapaya

    (University of Oxford
    University of Oxford)

  • Teresa Lambe

    (University of Oxford
    University of Oxford)

  • Dan Wootton

    (University of Liverpool
    Liverpool University Hospitals NHS Foundation Trust
    University of Liverpool)

  • Victoria Hall

    (UK Health Security Agency
    Imperial College London)

  • Susan Hopkins

    (UK Health Security Agency
    Imperial College London
    University of Oxford)

  • Tao Dong

    (University of Oxford
    University of Oxford
    University of Oxford)

  • Eleanor Barnes

    (University of Oxford
    Oxford NIHR Biomedical Research Centre and Oxford University NHS Foundation Trust)

  • Gavin Screaton

    (University of Oxford
    University of Oxford)

  • Alex Richter

    (University of Birmingham
    University Hospitals Birmingham NHS Foundation Trust)

  • Lance Turtle

    (University of Liverpool
    Liverpool University Hospitals NHS Foundation Trust (member of Liverpool Health Partners))

  • Sarah L. Rowland-Jones

    (The University of Sheffield
    Sheffield Teaching Hospitals NHS Foundation Trust)

  • Miles Carroll

    (University of Oxford
    University of Oxford)

  • Christopher J. A. Duncan

    (Newcastle University
    Newcastle upon Tyne Hospitals NHS Foundation Trust)

  • Paul Klenerman

    (University of Oxford
    Oxford NIHR Biomedical Research Centre and Oxford University NHS Foundation Trust
    University of Oxford)

  • Susanna J. Dunachie

    (University of Oxford
    University of Oxford
    Oxford NIHR Biomedical Research Centre and Oxford University NHS Foundation Trust
    Mahidol University)

  • Rebecca P. Payne

    (Newcastle University)

  • Thushan I. Silva

    (The University of Sheffield
    Sheffield Teaching Hospitals NHS Foundation Trust
    Medical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine)

Abstract

Pronounced immune escape by the SARS-CoV-2 Omicron variant has resulted in many individuals possessing hybrid immunity, generated through a combination of vaccination and infection. Concerns have been raised that omicron breakthrough infections in triple-vaccinated individuals result in poor induction of omicron-specific immunity, and that prior SARS-CoV-2 infection is associated with immune dampening. Taking a broad and comprehensive approach, we characterize mucosal and blood immunity to spike and non-spike antigens following BA.1/BA.2 infections in triple mRNA-vaccinated individuals, with and without prior SARS-CoV-2 infection. We find that most individuals increase BA.1/BA.2/BA.5-specific neutralizing antibodies following infection, but confirm that the magnitude of increase and post-omicron titres are higher in the infection-naive. In contrast, significant increases in nasal responses, including neutralizing activity against BA.5 spike, are seen regardless of infection history. Spike-specific T cells increase only in infection-naive vaccinees; however, post-omicron T cell responses are significantly higher in the previously-infected, who display a maximally induced response with a highly cytotoxic CD8+ phenotype following their 3rd mRNA vaccine dose. Responses to non-spike antigens increase significantly regardless of prior infection status. These findings suggest that hybrid immunity induced by omicron breakthrough infections is characterized by significant immune enhancement that can help protect against future omicron variants.

Suggested Citation

  • Hailey Hornsby & Alexander R. Nicols & Stephanie Longet & Chang Liu & Adriana Tomic & Adrienn Angyal & Barbara Kronsteiner & Jessica K. Tyerman & Tom Tipton & Peijun Zhang & Marta Gallis & Piyada Supa, 2023. "Omicron infection following vaccination enhances a broad spectrum of immune responses dependent on infection history," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40592-4
    DOI: 10.1038/s41467-023-40592-4
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    References listed on IDEAS

    as
    1. Raquel Viana & Sikhulile Moyo & Daniel G. Amoako & Houriiyah Tegally & Cathrine Scheepers & Christian L. Althaus & Ugochukwu J. Anyaneji & Phillip A. Bester & Maciej F. Boni & Mohammed Chand & Wonderf, 2022. "Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa," Nature, Nature, vol. 603(7902), pages 679-686, March.
    2. Delphine Planas & Nell Saunders & Piet Maes & Florence Guivel-Benhassine & Cyril Planchais & Julian Buchrieser & William-Henry Bolland & Françoise Porrot & Isabelle Staropoli & Frederic Lemoine & Hélè, 2022. "Considerable escape of SARS-CoV-2 Omicron to antibody neutralization," Nature, Nature, vol. 602(7898), pages 671-675, February.
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    Cited by:

    1. Jernej Pušnik & Jasmin Zorn & Werner O. Monzon-Posadas & Kathrin Peters & Emmanuil Osypchuk & Sabine Blaschke & Hendrik Streeck, 2024. "Vaccination impairs de novo immune response to omicron breakthrough infection, a precondition for the original antigenic sin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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