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Correlates of protection against SARS-CoV-2 in rhesus macaques

Author

Listed:
  • Katherine McMahan

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Jingyou Yu

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Noe B. Mercado

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Carolin Loos

    (Ragon Institute of MGH, MIT and Harvard
    Massachusetts Institute of Technology)

  • Lisa H. Tostanoski

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Abishek Chandrashekar

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Jinyan Liu

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Lauren Peter

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Caroline Atyeo

    (Ragon Institute of MGH, MIT and Harvard
    Harvard Medical School)

  • Alex Zhu

    (Ragon Institute of MGH, MIT and Harvard)

  • Esther A. Bondzie

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Gabriel Dagotto

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School
    Harvard Medical School)

  • Makda S. Gebre

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School
    Harvard Medical School)

  • Catherine Jacob-Dolan

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School
    Harvard Medical School)

  • Zhenfeng Li

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Felix Nampanya

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Shivani Patel

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Laurent Pessaint

    (Bioqual)

  • Alex Ry

    (Bioqual)

  • Kelvin Blade

    (Bioqual)

  • Jake Yalley-Ogunro

    (Bioqual)

  • Mehtap Cabus

    (Bioqual)

  • Renita Brown

    (Bioqual)

  • Anthony Cook

    (Bioqual)

  • Elyse Teow

    (Bioqual)

  • Hanne Andersen

    (Bioqual)

  • Mark G. Lewis

    (Bioqual)

  • Douglas A. Lauffenburger

    (Massachusetts Institute of Technology)

  • Galit Alter

    (Ragon Institute of MGH, MIT and Harvard
    Massachusetts Consortium on Pathogen Readiness)

  • Dan H. Barouch

    (Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School
    Ragon Institute of MGH, MIT and Harvard
    Harvard Medical School
    Massachusetts Consortium on Pathogen Readiness)

Abstract

Recent studies have reported the protective efficacy of both natural1 and vaccine-induced2–7 immunity against challenge with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in rhesus macaques. However, the importance of humoral and cellular immunity for protection against infection with SARS-CoV-2 remains to be determined. Here we show that the adoptive transfer of purified IgG from convalescent rhesus macaques (Macaca mulatta) protects naive recipient macaques against challenge with SARS-CoV-2 in a dose-dependent fashion. Depletion of CD8+ T cells in convalescent macaques partially abrogated the protective efficacy of natural immunity against rechallenge with SARS-CoV-2, which suggests a role for cellular immunity in the context of waning or subprotective antibody titres. These data demonstrate that relatively low antibody titres are sufficient for protection against SARS-CoV-2 in rhesus macaques, and that cellular immune responses may contribute to protection if antibody responses are suboptimal. We also show that higher antibody titres are required for treatment of SARS-CoV-2 infection in macaques. These findings have implications for the development of SARS-CoV-2 vaccines and immune-based therapeutic agents.

Suggested Citation

  • Katherine McMahan & Jingyou Yu & Noe B. Mercado & Carolin Loos & Lisa H. Tostanoski & Abishek Chandrashekar & Jinyan Liu & Lauren Peter & Caroline Atyeo & Alex Zhu & Esther A. Bondzie & Gabriel Dagott, 2021. "Correlates of protection against SARS-CoV-2 in rhesus macaques," Nature, Nature, vol. 590(7847), pages 630-634, February.
    • Handle: RePEc:nat:nature:v:590:y:2021:i:7847:d:10.1038_s41586-020-03041-6
    DOI: 10.1038/s41586-020-03041-6
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    Cited by:

    1. Ramon Roozendaal & Laura Solforosi & Daniel J. Stieh & Jan Serroyen & Roel Straetemans & Anna Dari & Muriel Boulton & Frank Wegmann & Sietske K. Rosendahl Huber & Joan E. M. van der Lubbe & Jenny Hend, 2021. "SARS-CoV-2 binding and neutralizing antibody levels after Ad26.COV2.S vaccination predict durable protection in rhesus macaques," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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    6. Payton A.-B. Weidenbacher & Mrinmoy Sanyal & Natalia Friedland & Shaogeng Tang & Prabhu S. Arunachalam & Mengyun Hu & Ozan S. Kumru & Mary Kate Morris & Jane Fontenot & Lisa Shirreff & Jonathan Do & Y, 2023. "A ferritin-based COVID-19 nanoparticle vaccine that elicits robust, durable, broad-spectrum neutralizing antisera in non-human primates," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. 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.
    8. Christine D. Palmer & Ciaran D. Scallan & Lauren D. Kraemer Tardif & Melissa A. Kachura & Amy R. Rappaport & Daniel O. Koralek & Alison Uriel & Leonid Gitlin & Joshua Klein & Matthew J. Davis & Harshn, 2023. "GRT-R910: a self-amplifying mRNA SARS-CoV-2 vaccine boosts immunity for ≥6 months in previously-vaccinated older adults," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Vincent Pavot & Catherine Berry & Michael Kishko & Natalie G. Anosova & Lu Li & Tim Tibbitts & Dean Huang & Alice Raillard & Sylviane Gautheron & Cindy Gutzeit & Marguerite Koutsoukos & Roman M. Chicz, 2023. "Beta variant COVID-19 protein booster vaccine elicits durable cross-neutralization against SARS-CoV-2 variants in non-human primates," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    10. Rúbens Prince dos Santos Alves & Julia Timis & Robyn Miller & Kristen Valentine & Paolla Beatriz Almeida Pinto & Andrew Gonzalez & Jose Angel Regla-Nava & Erin Maule & Michael N. Nguyen & Norazizah Sh, 2024. "Human coronavirus OC43-elicited CD4+ T cells protect against SARS-CoV-2 in HLA transgenic mice," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Philipe Gobeil & Stéphane Pillet & Iohann Boulay & Nathalie Charland & Aurélien Lorin & Matthew P. Cheng & Donald C. Vinh & Philippe Boutet & Robbert Most & François Roman & Maria Angeles Ceregido & N, 2022. "Durability and cross-reactivity of immune responses induced by a plant-based virus-like particle vaccine for COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    12. Aloysious Ssemaganda & Huong Mai Nguyen & Faisal Nuhu & Naima Jahan & Catherine M. Card & Sandra Kiazyk & Giulia Severini & Yoav Keynan & Ruey-Chyi Su & Hezhao Ji & Bernard Abrenica & Paul J. McLaren , 2022. "Expansion of cytotoxic tissue-resident CD8+ T cells and CCR6+CD161+ CD4+ T cells in the nasal mucosa following mRNA COVID-19 vaccination," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    13. Elham Khatamzas & Markus H. Antwerpen & Alexandra Rehn & Alexander Graf & Johannes Christian Hellmuth & Alexandra Hollaus & Anne-Wiebe Mohr & Erik Gaitzsch & Tobias Weiglein & Enrico Georgi & Clemens , 2022. "Accumulation of mutations in antibody and CD8 T cell epitopes in a B cell depleted lymphoma patient with chronic SARS-CoV-2 infection," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    14. Tomer Hertz & Shlomia Levy & Daniel Ostrovsky & Hanna Oppenheimer & Shosh Zismanov & Alona Kuzmina & Lilach M. Friedman & Sanja Trifkovic & David Brice & Lin Chun-Yang & Liel Cohen-Lavi & Yonat Shemer, 2023. "Correlates of protection for booster doses of the SARS-CoV-2 vaccine BNT162b2," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Dapeng Li & David R. Martinez & Alexandra Schäfer & Haiyan Chen & Maggie Barr & Laura L. Sutherland & Esther Lee & Robert Parks & Dieter Mielke & Whitney Edwards & Amanda Newman & Kevin W. Bock & Mahn, 2022. "Breadth of SARS-CoV-2 neutralization and protection induced by a nanoparticle vaccine," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. 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.
    17. Adriana Tomic & Donal T. Skelly & Ane Ogbe & Daniel O’Connor & Matthew Pace & Emily Adland & Frances Alexander & Mohammad Ali & Kirk Allott & M. Azim Ansari & Sandra Belij-Rammerstorfer & Sagida Bibi , 2022. "Divergent trajectories of antiviral memory after SARS-CoV-2 infection," Nature Communications, Nature, vol. 13(1), pages 1-20, December.

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