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

Hornsby, Hailey; Nicols, Alexander R.; Longet, Stephanie; Liu, Chang; Tomic, Adriana; Angyal, Adrienn; Kronsteiner, Barbara; Tyerman, Jessica K.; Tipton, Tom; Zhang, Peijun; Gallis, Marta; Supasa, Piyada; Selvaraj, Muneeswaran; Abraham, Priyanka; Neale, Isabel; Ali, Mohammad; Barratt, Natalie A.; Nell, Jeremy M.; Gustafsson, Lotta; Strickland, Scarlett; Grouneva, Irina; Rostron, Timothy; Moore, Shona C.; Hering, Luisa M.; Dobson, Susan L.; Bibi, Sagida; Mongkolsapaya, Juthathip; Lambe, Teresa; Wootton, Dan; Hall, Victoria; Hopkins, Susan; Dong, Tao; Barnes, Eleanor; Screaton, Gavin; Richter, Alex; Turtle, Lance; Rowland-Jones, Sarah L.; Carroll, Miles; Duncan, Christopher J. A.; Klenerman, Paul; Dunachie, Susanna J.; Payne, Rebecca P.; Silva, Thushan I.

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

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 Supasa, Muneeswaran Selvaraj, Priyanka Abraham, Isabel Neale, Mohammad Ali, Natalie A. Barratt, Jeremy M. Nell, Lotta Gustafsson, Scarlett Strickland, Irina Grouneva, Timothy Rostron, Shona C. Moore, Luisa M. Hering, Susan L. Dobson, Sagida Bibi, Juthathip Mongkolsapaya, Teresa Lambe, Dan Wootton, Victoria Hall, Susan Hopkins, Tao Dong, Eleanor Barnes, Gavin Screaton, Alex Richter, Lance Turtle, Sarah L. Rowland-Jones, Miles Carroll, Christopher J. A. Duncan, Paul Klenerman (), Susanna J. Dunachie, Rebecca P. Payne and Thushan I. Silva ()
Additional contact information
Hailey Hornsby: The University of Sheffield
Alexander R. Nicols: Newcastle University
Stephanie Longet: University of Oxford
Chang Liu: University of Oxford
Adriana Tomic: Boston University
Adrienn Angyal: The University of Sheffield
Barbara Kronsteiner: University of Oxford
Jessica K. Tyerman: Newcastle University
Tom Tipton: 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
Isabel Neale: University of Oxford
Mohammad Ali: University of Oxford
Natalie A. Barratt: The University of Sheffield
Jeremy M. Nell: Newcastle University
Lotta Gustafsson: The University of Sheffield
Scarlett Strickland: The University of Sheffield
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
Teresa Lambe: University of Oxford
Dan Wootton: University of Liverpool
Victoria Hall: UK Health Security Agency
Susan Hopkins: UK Health Security Agency
Tao Dong: University of Oxford
Eleanor Barnes: University of Oxford
Gavin Screaton: University of Oxford
Alex Richter: University of Birmingham
Lance Turtle: University of Liverpool
Sarah L. Rowland-Jones: The University of Sheffield
Miles Carroll: University of Oxford
Christopher J. A. Duncan: Newcastle University
Paul Klenerman: University of Oxford
Susanna J. Dunachie: University of Oxford
Rebecca P. Payne: Newcastle University
Thushan I. Silva: The University of Sheffield

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-40592-4

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