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SARS-CoV-2 vaccination elicits broad and potent antibody effector functions to variants of concern in vulnerable populations

Author

Listed:
  • Andrew P. Hederman

    (Dartmouth College)

  • Harini Natarajan

    (Dartmouth College)

  • Leo Heyndrickx

    (Institute of Tropical Medicine)

  • Kevin K. Ariën

    (Institute of Tropical Medicine)

  • Joshua A. Wiener

    (Dartmouth College)

  • Peter F. Wright

    (Dartmouth-Hitchcock Medical Center)

  • Evan M. Bloch

    (Johns Hopkins School of Medicine)

  • Aaron A. R. Tobian

    (Johns Hopkins School of Medicine)

  • Andrew D. Redd

    (Johns Hopkins School of Medicine
    Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Joel N. Blankson

    (Johns Hopkins School of Medicine)

  • Amihai Rottenstreich

    (Hadassah-Hebrew University Medical Center)

  • Gila Zarbiv

    (Hadassah University Medical Center)

  • Dana Wolf

    (Hadassah University Medical Center)

  • Tessa Goetghebuer

    (Université libre de Bruxelles
    CHU St Pierre)

  • Arnaud Marchant

    (Université libre de Bruxelles)

  • Margaret E. Ackerman

    (Dartmouth College
    Dartmouth College)

Abstract

SARS-CoV-2 variants have continuously emerged in the face of effective vaccines. Reduced neutralization against variants raises questions as to whether other antibody functions are similarly compromised, or if they might compensate for lost neutralization activity. Here, the breadth and potency of antibody recognition and effector function is surveyed following either infection or vaccination. Considering pregnant women as a model cohort with higher risk of severe illness and death, we observe similar binding and functional breadth for healthy and immunologically vulnerable populations, but considerably greater functional antibody breadth and potency across variants associated with vaccination. In contrast, greater antibody functional activity targeting the endemic coronavirus OC43 is noted among convalescent individuals, illustrating a dichotomy in recognition between close and distant human coronavirus strains associated with exposure history. This analysis of antibody functions suggests the differential potential for antibody effector functions to contribute to protecting vaccinated and convalescent subjects as novel variants continue to evolve.

Suggested Citation

  • Andrew P. Hederman & Harini Natarajan & Leo Heyndrickx & Kevin K. Ariën & Joshua A. Wiener & Peter F. Wright & Evan M. Bloch & Aaron A. R. Tobian & Andrew D. Redd & Joel N. Blankson & Amihai Rottenstr, 2023. "SARS-CoV-2 vaccination elicits broad and potent antibody effector functions to variants of concern in vulnerable populations," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40960-0
    DOI: 10.1038/s41467-023-40960-0
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    1. Li Wang & Markus H. Kainulainen & Nannan Jiang & Han Di & Gaston Bonenfant & Lisa Mills & Michael Currier & Punya Shrivastava-Ranjan & Brenda M. Calderon & Mili Sheth & Brian R. Mann & Jaber Hossain &, 2022. "Differential neutralization and inhibition of SARS-CoV-2 variants by antibodies elicited by COVID-19 mRNA vaccines," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Prabhu S. Arunachalam & Madeleine K. D. Scott & Thomas Hagan & Chunfeng Li & Yupeng Feng & Florian Wimmers & Lilit Grigoryan & Meera Trisal & Venkata Viswanadh Edara & Lilin Lai & Sarah Esther Chang &, 2021. "Systems vaccinology of the BNT162b2 mRNA vaccine in humans," Nature, Nature, vol. 596(7872), pages 410-416, August.
    3. Chunyan Wang & Emma L. Hesketh & Tatiana M. Shamorkina & Wentao Li & Peter J. Franken & Dubravka Drabek & Rien Haperen & Sarah Townend & Frank J. M. Kuppeveld & Frank Grosveld & Neil A. Ranson & Joost, 2022. "Antigenic structure of the human coronavirus OC43 spike reveals exposed and occluded neutralizing epitopes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Dora Pinto & Young-Jun Park & Martina Beltramello & Alexandra C. Walls & M. Alejandra Tortorici & Siro Bianchi & Stefano Jaconi & Katja Culap & Fabrizia Zatta & Anna De Marco & Alessia Peter & Barbara, 2020. "Cross-neutralization of SARS-CoV-2 by a human monoclonal SARS-CoV antibody," Nature, Nature, vol. 583(7815), pages 290-295, July.
    5. Zijun Wang & Frauke Muecksch & Dennis Schaefer-Babajew & Shlomo Finkin & Charlotte Viant & Christian Gaebler & Hans- Heinrich Hoffmann & Christopher O. Barnes & Melissa Cipolla & Victor Ramos & Thiago, 2021. "Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection," Nature, Nature, vol. 595(7867), pages 426-431, July.
    6. Carolina Lucas & Chantal B. F. Vogels & Inci Yildirim & Jessica E. Rothman & Peiwen Lu & Valter Monteiro & Jeff R. Gehlhausen & Melissa Campbell & Julio Silva & Alexandra Tabachnikova & Mario A. Peña-, 2021. "Impact of circulating SARS-CoV-2 variants on mRNA vaccine-induced immunity," Nature, Nature, vol. 600(7889), pages 523-529, December.
    7. Pengfei Wang & Manoj S. Nair & Lihong Liu & Sho Iketani & Yang Luo & Yicheng Guo & Maple Wang & Jian Yu & Baoshan Zhang & Peter D. Kwong & Barney S. Graham & John R. Mascola & Jennifer Y. Chang & Mich, 2021. "Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7," Nature, Nature, vol. 593(7857), pages 130-135, May.
    8. Rachel Yamin & Andrew T. Jones & Hans-Heinrich Hoffmann & Alexandra Schäfer & Kevin S. Kao & Rebecca L. Francis & Timothy P. Sheahan & Ralph S. Baric & Charles M. Rice & Jeffrey V. Ravetch & Stylianos, 2021. "Fc-engineered antibody therapeutics with improved anti-SARS-CoV-2 efficacy," Nature, Nature, vol. 599(7885), pages 465-470, November.
    9. Davide F. Robbiani & Christian Gaebler & Frauke Muecksch & Julio C. C. Lorenzi & Zijun Wang & Alice Cho & Marianna Agudelo & Christopher O. Barnes & Anna Gazumyan & Shlomo Finkin & Thomas Hägglöf & Th, 2020. "Convergent antibody responses to SARS-CoV-2 in convalescent individuals," Nature, Nature, vol. 584(7821), pages 437-442, August.
    10. Timothy A. Bates & Hans C. Leier & Zoe L. Lyski & Savannah K. McBride & Felicity J. Coulter & Jules B. Weinstein & James R. Goodman & Zhengchun Lu & Sarah A. R. Siegel & Peter Sullivan & Matt Strnad &, 2021. "Neutralization of SARS-CoV-2 variants by convalescent and BNT162b2 vaccinated serum," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    11. Zijun Wang & Fabian Schmidt & Yiska Weisblum & Frauke Muecksch & Christopher O. Barnes & Shlomo Finkin & Dennis Schaefer-Babajew & Melissa Cipolla & Christian Gaebler & Jenna A. Lieberman & Thiago Y. , 2021. "mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants," Nature, Nature, vol. 592(7855), pages 616-622, April.
    Full references (including those not matched with items on IDEAS)

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