IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38810-0.html
   My bibliography  Save this article

Age-associated B cells predict impaired humoral immunity after COVID-19 vaccination in patients receiving immune checkpoint blockade

Author

Listed:
  • Juan Carlos Yam-Puc

    (University of Cambridge)

  • Zhaleh Hosseini

    (University of Cambridge)

  • Emily C. Horner

    (University of Cambridge)

  • Pehuén Pereyra Gerber

    (University of Cambridge
    University of Cambridge)

  • Nonantzin Beristain-Covarrubias

    (University of Cambridge)

  • Robert Hughes

    (University of Cambridge)

  • Aleksei Lulla

    (University of Cambridge)

  • Maria Rust

    (University of Cambridge)

  • Rebecca Boston

    (University of Cambridge)

  • Magda Ali

    (University of Cambridge)

  • Katrin Fischer

    (University of Cambridge)

  • Edward Simmons-Rosello

    (University of Cambridge)

  • Martin O’Reilly

    (University of Cambridge)

  • Harry Robson

    (University of Cambridge)

  • Lucy H. Booth

    (University of Cambridge)

  • Lakmini Kahanawita

    (University of Cambridge)

  • Andrea Correa-Noguera

    (Cambridge University NHS Hospitals Foundation Trust)

  • David Favara

    (Cambridge University NHS Hospitals Foundation Trust)

  • Lourdes Ceron-Gutierrez

    (Cambridge University NHS Hospitals Foundation Trust)

  • Baerbel Keller

    (University of Freiburg
    University of Freiburg)

  • Andrew Craxton

    (University of Cambridge)

  • Georgina S. F. Anderson

    (University of Cambridge)

  • Xiao-Ming Sun

    (University of Cambridge)

  • Anne Elmer

    (NIHR Cambridge Clinical Research Facility)

  • Caroline Saunders

    (NIHR Cambridge Clinical Research Facility)

  • Areti Bermperi

    (NIHR Cambridge Clinical Research Facility)

  • Sherly Jose

    (NIHR Cambridge Clinical Research Facility)

  • Nathalie Kingston

    (Cambridge University Hospitals NHS Foundation Trust)

  • Thomas E. Mulroney

    (University of Cambridge)

  • Lucia P. G. Piñon

    (University of Cambridge)

  • Michael A. Chapman

    (University of Cambridge)

  • Sofia Grigoriadou

    (Barts Health)

  • Marion MacFarlane

    (University of Cambridge)

  • Anne E. Willis

    (University of Cambridge)

  • Kiran R. Patil

    (University of Cambridge)

  • Sarah Spencer

    (University of Cambridge)

  • Emily Staples

    (University of Cambridge
    Cambridge University NHS Hospitals Foundation Trust)

  • Klaus Warnatz

    (University of Freiburg
    University of Freiburg
    University Hospital Zurich)

  • Matthew S. Buckland

    (Barts Health
    Section of Cellular and Molecular Immunology)

  • Florian Hollfelder

    (University of Cambridge)

  • Marko Hyvönen

    (University of Cambridge)

  • Rainer Döffinger

    (Cambridge University NHS Hospitals Foundation Trust)

  • Christine Parkinson

    (Cambridge University NHS Hospitals Foundation Trust)

  • Sara Lear

    (Cambridge University NHS Hospitals Foundation Trust)

  • Nicholas J. Matheson

    (University of Cambridge
    University of Cambridge
    NHS Blood and Transplant)

  • James E. D. Thaventhiran

    (University of Cambridge
    Cambridge University NHS Hospitals Foundation Trust)

Abstract

Age-associated B cells (ABC) accumulate with age and in individuals with different immunological disorders, including cancer patients treated with immune checkpoint blockade and those with inborn errors of immunity. Here, we investigate whether ABCs from different conditions are similar and how they impact the longitudinal level of the COVID-19 vaccine response. Single-cell RNA sequencing indicates that ABCs with distinct aetiologies have common transcriptional profiles and can be categorised according to their expression of immune genes, such as the autoimmune regulator (AIRE). Furthermore, higher baseline ABC frequency correlates with decreased levels of antigen-specific memory B cells and reduced neutralising capacity against SARS-CoV-2. ABCs express high levels of the inhibitory FcγRIIB receptor and are distinctive in their ability to bind immune complexes, which could contribute to diminish vaccine responses either directly, or indirectly via enhanced clearance of immune complexed-antigen. Expansion of ABCs may, therefore, serve as a biomarker identifying individuals at risk of suboptimal responses to vaccination.

Suggested Citation

  • Juan Carlos Yam-Puc & Zhaleh Hosseini & Emily C. Horner & Pehuén Pereyra Gerber & Nonantzin Beristain-Covarrubias & Robert Hughes & Aleksei Lulla & Maria Rust & Rebecca Boston & Magda Ali & Katrin Fis, 2023. "Age-associated B cells predict impaired humoral immunity after COVID-19 vaccination in patients receiving immune checkpoint blockade," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38810-0
    DOI: 10.1038/s41467-023-38810-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38810-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38810-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Dami A. Collier & Isabella A. T. M. Ferreira & Prasanti Kotagiri & Rawlings P. Datir & Eleanor Y. Lim & Emma Touizer & Bo Meng & Adam Abdullahi & Anne Elmer & Nathalie Kingston & Barbara Graves & Emma, 2021. "Age-related immune response heterogeneity to SARS-CoV-2 vaccine BNT162b2," Nature, Nature, vol. 596(7872), pages 417-422, August.
    2. Matthew S. Buckland & James B. Galloway & Caoimhe Nic Fhogartaigh & Luke Meredith & Nicholas M. Provine & Stuart Bloor & Ane Ogbe & Wioleta M. Zelek & Anna Smielewska & Anna Yakovleva & Tiffeney Mann , 2020. "Treatment of COVID-19 with remdesivir in the absence of humoral immunity: a case report," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Kevin J. Kramer & Erin M. Wilfong & Kelsey Voss & Sierra M. Barone & Andrea R. Shiakolas & Nagarajan Raju & Caroline E. Roe & Naveenchandra Suryadevara & Lauren M. Walker & Steven C. Wall & Ariana Pau, 2022. "Single-cell profiling of the antigen-specific response to BNT162b2 SARS-CoV-2 RNA vaccine," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Eva Stadler & Martin T. Burgess & Timothy E. Schlub & Shanchita R. Khan & Khai Li Chai & Zoe K. McQuilten & Erica M. Wood & Mark N. Polizzotto & Stephen J. Kent & Deborah Cromer & Miles P. Davenport &, 2023. "Monoclonal antibody levels and protection from COVID-19," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    3. Sebastian Weigang & Jonas Fuchs & Gert Zimmer & Daniel Schnepf & Lisa Kern & Julius Beer & Hendrik Luxenburger & Jakob Ankerhold & Valeria Falcone & Janine Kemming & Maike Hofmann & Robert Thimme & Ch, 2021. "Within-host evolution of SARS-CoV-2 in an immunosuppressed COVID-19 patient as a source of immune escape variants," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    4. Adam Abdullahi & David Oladele & Michael Owusu & Steven A. Kemp & James Ayorinde & Abideen Salako & Douglas Fink & Fehintola Ige & Isabella A. T. M. Ferreira & Bo Meng & Augustina Angelina Sylverken &, 2022. "SARS-COV-2 antibody responses to AZD1222 vaccination in West Africa," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Laurent Renia & Yun Shan Goh & Angeline Rouers & Nina Bert & Wan Ni Chia & Jean-Marc Chavatte & Siew‐Wai Fong & Zi Wei Chang & Nicole Ziyi Zhuo & Matthew Zirui Tay & Yi-Hao Chan & Chee Wah Tan & Nicho, 2022. "Lower vaccine-acquired immunity in the elderly population following two-dose BNT162b2 vaccination is alleviated by a third vaccine dose," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Jae Sung Lim & Eun Jae Jeon & Hye Sun Go & Hyung-Jin Kim & Kye Young Kim & Thi Quynh Trang Nguyen & Da Young Lee & Kyu Suk Kim & Federico Pietrocola & Seol Hee Hong & Shee Eun Lee & Kyoung-Shim Kim & , 2024. "Mucosal TLR5 activation controls healthspan and longevity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Helen Ward & Matthew Whitaker & Barnaby Flower & Sonja N. Tang & Christina Atchison & Ara Darzi & Christl A. Donnelly & Alexandra Cann & Peter J. Diggle & Deborah Ashby & Steven Riley & Wendy S. Barcl, 2022. "Population antibody responses following COVID-19 vaccination in 212,102 individuals," Nature Communications, Nature, vol. 13(1), pages 1-6, December.
    8. Gayatri Amirthalingam & Jamie Lopez Bernal & Nick J. Andrews & Heather Whitaker & Charlotte Gower & Julia Stowe & Elise Tessier & Sathyavani Subbarao & Georgina Ireland & Frances Baawuah & Ezra Linley, 2021. "Serological responses and vaccine effectiveness for extended COVID-19 vaccine schedules in England," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    9. Matt D. T. Hitchings & Otavio T. Ranzani & Murilo Dorion & Tatiana Lang D’Agostini & Regiane Cardoso de Paula & Olivia Ferreira Pereira de Paula & Edlaine Faria de Moura Villela & Mario Sergio Scaramu, 2021. "Effectiveness of ChAdOx1 vaccine in older adults during SARS-CoV-2 Gamma variant circulation in São Paulo," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    10. Daan K. J. Pieren & Sebastián G. Kuguel & Joel Rosado & Alba G. Robles & Joan Rey-Cano & Cristina Mancebo & Juliana Esperalba & Vicenç Falcó & María J. Buzón & Meritxell Genescà, 2023. "Limited induction of polyfunctional lung-resident memory T cells against SARS-CoV-2 by mRNA vaccination compared to infection," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Zhencui Li & Pei Hu & Lin Qu & Mingda Yang & Ming Qiu & Chunyan Xie & Haiyi Yang & Jiadian Cao & Lina Yi & Zhe Liu & Lirong Zou & Huimin Lian & Huiling Zeng & Shaojian Xu & Pengwei Hu & Jiufeng Sun & , 2024. "Molecular epidemiology and population immunity of SARS-CoV-2 in Guangdong (2022–2023) following a pivotal shift in the pandemic," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38810-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.