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Primary exposure to SARS-CoV-2 variants elicits convergent epitope specificities, immunoglobulin V gene usage and public B cell clones

Author

Listed:
  • Noemia S. Lima

    (National Institutes of Health)

  • Maryam Musayev

    (National Institutes of Health)

  • Timothy S. Johnston

    (National Institutes of Health)

  • Danielle A. Wagner

    (National Institutes of Health)

  • Amy R. Henry

    (National Institutes of Health)

  • Lingshu Wang

    (National Institutes of Health)

  • Eun Sung Yang

    (National Institutes of Health)

  • Yi Zhang

    (National Institutes of Health)

  • Kevina Birungi

    (National Institutes of Health)

  • Walker P. Black

    (National Institutes of Health)

  • Sijy O’Dell

    (National Institutes of Health)

  • Stephen D. Schmidt

    (National Institutes of Health)

  • Damee Moon

    (National Institutes of Health)

  • Cynthia G. Lorang

    (National Institutes of Health)

  • Bingchun Zhao

    (National Institutes of Health)

  • Man Chen

    (National Institutes of Health)

  • Kristin L. Boswell

    (National Institutes of Health)

  • Jesmine Roberts-Torres

    (National Institutes of Health)

  • Rachel L. Davis

    (National Institutes of Health)

  • Lowrey Peyton

    (National Institutes of Health)

  • Sandeep R. Narpala

    (National Institutes of Health)

  • Sarah O’Connell

    (National Institutes of Health)

  • Leonid Serebryannyy

    (National Institutes of Health)

  • Jennifer Wang

    (National Institutes of Health)

  • Alexander Schrager

    (National Institutes of Health)

  • Chloe Adrienna Talana

    (National Institutes of Health)

  • Geoffrey Shimberg

    (National Institutes of Health)

  • Kwanyee Leung

    (National Institutes of Health)

  • Wei Shi

    (National Institutes of Health)

  • Rawan Khashab

    (Sheba Medical Center)

  • Asaf Biber

    (Sheba Medical Center
    Tel Aviv University)

  • Tal Zilberman

    (Sheba Medical Center
    Tel Aviv University)

  • Joshua Rhein

    (University of Minnesota Medical School)

  • Sara Vetter

    (Minnesota Department of Health)

  • Afeefa Ahmed

    (University of Minnesota Medical School)

  • Laura Novik

    (National Institutes of Health)

  • Alicia Widge

    (National Institutes of Health)

  • Ingelise Gordon

    (National Institutes of Health)

  • Mercy Guech

    (National Institutes of Health)

  • I-Ting Teng

    (National Institutes of Health)

  • Emily Phung

    (National Institutes of Health)

  • Tracy J. Ruckwardt

    (National Institutes of Health)

  • Amarendra Pegu

    (National Institutes of Health)

  • John Misasi

    (National Institutes of Health)

  • Nicole A. Doria-Rose

    (National Institutes of Health)

  • Martin Gaudinski

    (National Institutes of Health)

  • Richard A. Koup

    (National Institutes of Health)

  • Peter D. Kwong

    (National Institutes of Health)

  • Adrian B. McDermott

    (National Institutes of Health)

  • Sharon Amit

    (Sheba Medical Center)

  • Timothy W. Schacker

    (University of Minnesota Medical School)

  • Itzchak Levy

    (Sheba Medical Center
    Tel Aviv University)

  • John R. Mascola

    (National Institutes of Health)

  • Nancy J. Sullivan

    (National Institutes of Health)

  • Chaim A. Schramm

    (National Institutes of Health)

  • Daniel C. Douek

    (National Institutes of Health)

Abstract

An important consequence of infection with a SARS-CoV-2 variant is protective humoral immunity against other variants. However, the basis for such cross-protection at the molecular level is incompletely understood. Here, we characterized the repertoire and epitope specificity of antibodies elicited by infection with the Beta, Gamma and WA1 ancestral variants and assessed their cross-reactivity to these and the more recent Delta and Omicron variants. We developed a method to obtain immunoglobulin sequences with concurrent rapid production and functional assessment of monoclonal antibodies from hundreds of single B cells sorted by flow cytometry. Infection with any variant elicited similar cross-binding antibody responses exhibiting a conserved hierarchy of epitope immunodominance. Furthermore, convergent V gene usage and similar public B cell clones were elicited regardless of infecting variant. These convergent responses despite antigenic variation may account for the continued efficacy of vaccines based on a single ancestral variant.

Suggested Citation

  • Noemia S. Lima & Maryam Musayev & Timothy S. Johnston & Danielle A. Wagner & Amy R. Henry & Lingshu Wang & Eun Sung Yang & Yi Zhang & Kevina Birungi & Walker P. Black & Sijy O’Dell & Stephen D. Schmid, 2022. "Primary exposure to SARS-CoV-2 variants elicits convergent epitope specificities, immunoglobulin V gene usage and public B cell clones," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35456-2
    DOI: 10.1038/s41467-022-35456-2
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    as
    1. Fabian Schmidt & Yiska Weisblum & Magdalena Rutkowska & Daniel Poston & Justin DaSilva & Fengwen Zhang & Eva Bednarski & Alice Cho & Dennis J. Schaefer-Babajew & Christian Gaebler & Marina Caskey & Mi, 2021. "High genetic barrier to SARS-CoV-2 polyclonal neutralizing antibody escape," Nature, Nature, vol. 600(7889), pages 512-516, December.
    2. Lihong Liu & Pengfei Wang & Manoj S. Nair & Jian Yu & Micah Rapp & Qian Wang & Yang Luo & Jasper F.-W. Chan & Vincent Sahi & Amir Figueroa & Xinzheng V. Guo & Gabriele Cerutti & Jude Bimela & Jason Go, 2020. "Potent neutralizing antibodies against multiple epitopes on SARS-CoV-2 spike," Nature, Nature, vol. 584(7821), pages 450-456, August.
    3. Yunlong Cao & Ayijiang Yisimayi & Fanchong Jian & Weiliang Song & Tianhe Xiao & Lei Wang & Shuo Du & Jing Wang & Qianqian Li & Xiaosu Chen & Yuanling Yu & Peng Wang & Zhiying Zhang & Pulan Liu & Ran A, 2022. "BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection," Nature, Nature, vol. 608(7923), pages 593-602, August.
    4. Ge Song & Wan-ting He & Sean Callaghan & Fabio Anzanello & Deli Huang & James Ricketts & Jonathan L. Torres & Nathan Beutler & Linghang Peng & Sirena Vargas & Jon Cassell & Mara Parren & Linlin Yang &, 2021. "Cross-reactive serum and memory B-cell responses to spike protein in SARS-CoV-2 and endemic coronavirus infection," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. 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.
    6. 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.
    7. Cinque Soto & Robin G. Bombardi & Andre Branchizio & Nurgun Kose & Pranathi Matta & Alexander M. Sevy & Robert S. Sinkovits & Pavlo Gilchuk & Jessica A. Finn & James E. Crowe, 2019. "High frequency of shared clonotypes in human B cell receptor repertoires," Nature, Nature, vol. 566(7744), pages 398-402, February.
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