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Vaccine-induced protection against SARS-CoV-2 requires IFN-γ-driven cellular immune response

Author

Listed:
  • Xiaolei Wang

    (The University of Hong Kong
    The University of Hong Kong-Shenzhen Hospital)

  • Terrence Tsz-Tai Yuen

    (The University of Hong Kong)

  • Ying Dou

    (The University of Hong Kong)

  • Jingchu Hu

    (The University of Hong Kong)

  • Renhao Li

    (The University of Hong Kong
    The University of Hong Kong)

  • Zheng Zeng

    (The University of Hong Kong)

  • Xuansheng Lin

    (The University of Hong Kong)

  • Huarui Gong

    (The University of Hong Kong)

  • Celia Hoi-Ching Chan

    (The University of Hong Kong)

  • Chaemin Yoon

    (The University of Hong Kong)

  • Huiping Shuai

    (The University of Hong Kong)

  • Deborah Tip-Yin Ho

    (The University of Hong Kong)

  • Ivan Fan-Ngai Hung

    (The University of Hong Kong
    The University of Hong Kong-Shenzhen Hospital)

  • Bao-Zhong Zhang

    (The University of Hong Kong
    Chinese Academy of Sciences)

  • Hin Chu

    (The University of Hong Kong
    The University of Hong Kong-Shenzhen Hospital
    The University of Hong Kong
    Hong Kong Science and Technology Park)

  • Jian-Dong Huang

    (The University of Hong Kong
    Chinese Academy of Sciences
    Sun Yat-Sen University
    The University of Hong Kong-Shenzhen Hospital)

Abstract

The overall success of worldwide mass vaccination in limiting the negative effect of the COVID-19 pandemics is inevitable, however, recent SARS-CoV-2 variants of concern, especially Omicron and its sub-lineages, efficiently evade humoral immunity mounted upon vaccination or previous infection. Thus, it is an important question whether these variants, or vaccines against them, induce anti-viral cellular immunity. Here we show that the mRNA vaccine BNT162b2 induces robust protective immunity in K18-hACE2 transgenic B-cell deficient (μMT) mice. We further demonstrate that the protection is attributed to cellular immunity depending on robust IFN-γ production. Viral challenge with SARS-CoV-2 Omicron BA.1 and BA.5.2 sub-variants induce boosted cellular responses in vaccinated μMT mice, which highlights the significance of cellular immunity against the ever-emerging SARS-CoV-2 variants evading antibody-mediated immunity. Our work, by providing evidence that BNT162b2 can induce significant protective immunity in mice that are unable to produce antibodies, thus highlights the importance of cellular immunity in the protection against SARS-CoV-2.

Suggested Citation

  • Xiaolei Wang & Terrence Tsz-Tai Yuen & Ying Dou & Jingchu Hu & Renhao Li & Zheng Zeng & Xuansheng Lin & Huarui Gong & Celia Hoi-Ching Chan & Chaemin Yoon & Huiping Shuai & Deborah Tip-Yin Ho & Ivan Fa, 2023. "Vaccine-induced protection against SARS-CoV-2 requires IFN-γ-driven cellular immune response," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39096-y
    DOI: 10.1038/s41467-023-39096-y
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    as
    1. Yunlong Cao & Jing Wang & Fanchong Jian & Tianhe Xiao & Weiliang Song & Ayijiang Yisimayi & Weijin Huang & Qianqian Li & Peng Wang & Ran An & Jing Wang & Yao Wang & Xiao Niu & Sijie Yang & Hui Liang &, 2022. "Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies," Nature, Nature, vol. 602(7898), pages 657-663, February.
    2. Huiping Shuai & Jasper Fuk-Woo Chan & Bingjie Hu & Yue Chai & Terrence Tsz-Tai Yuen & Feifei Yin & Xiner Huang & Chaemin Yoon & Jing-Chu Hu & Huan Liu & Jialu Shi & Yuanchen Liu & Tianrenzheng Zhu & J, 2022. "Attenuated replication and pathogenicity of SARS-CoV-2 B.1.1.529 Omicron," Nature, Nature, vol. 603(7902), pages 693-699, March.
    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. Johannes C. Melms & Jana Biermann & Huachao Huang & Yiping Wang & Ajay Nair & Somnath Tagore & Igor Katsyv & André F. Rendeiro & Amit Dipak Amin & Denis Schapiro & Chris J. Frangieh & Adrienne M. Luom, 2021. "Author Correction: A molecular single-cell lung atlas of lethal COVID-19," Nature, Nature, vol. 598(7882), pages 2-2, October.
    5. Lihong Liu & Sho Iketani & Yicheng Guo & Jasper F.-W. Chan & Maple Wang & Liyuan Liu & Yang Luo & Hin Chu & Yiming Huang & Manoj S. Nair & Jian Yu & Kenn K.-H. Chik & Terrence T.-T. Yuen & Chaemin Yoo, 2022. "Striking antibody evasion manifested by the Omicron variant of SARS-CoV-2," Nature, Nature, vol. 602(7898), pages 676-681, February.
    6. Hin Chu & Yuxin Hou & Dong Yang & Lei Wen & Huiping Shuai & Chaemin Yoon & Jialu Shi & Yue Chai & Terrence Tsz-Tai Yuen & Bingjie Hu & Cun Li & Xiaoyu Zhao & Yixin Wang & Xiner Huang & Kin Shing Lee &, 2022. "Coronaviruses exploit a host cysteine-aspartic protease for replication," Nature, Nature, vol. 609(7928), pages 785-792, September.
    7. Delphine Planas & Nell Saunders & Piet Maes & Florence Guivel-Benhassine & Cyril Planchais & Julian Buchrieser & William-Henry Bolland & Françoise Porrot & Isabelle Staropoli & Frederic Lemoine & Hélè, 2022. "Considerable escape of SARS-CoV-2 Omicron to antibody neutralization," Nature, Nature, vol. 602(7898), pages 671-675, February.
    8. Toni M. Delorey & Carly G. K. Ziegler & Graham Heimberg & Rachelly Normand & Yiming Yang & Åsa Segerstolpe & Domenic Abbondanza & Stephen J. Fleming & Ayshwarya Subramanian & Daniel T. Montoro & Karth, 2021. "COVID-19 tissue atlases reveal SARS-CoV-2 pathology and cellular targets," Nature, Nature, vol. 595(7865), pages 107-113, July.
    9. Jinyan Liu & Abishek Chandrashekar & Daniel Sellers & Julia Barrett & Catherine Jacob-Dolan & Michelle Lifton & Katherine McMahan & Michaela Sciacca & Haley VanWyk & Cindy Wu & Jingyou Yu & Ai-ris Y. , 2022. "Vaccines elicit highly conserved cellular immunity to SARS-CoV-2 Omicron," Nature, Nature, vol. 603(7901), pages 493-496, March.
    10. Johannes C. Melms & Jana Biermann & Huachao Huang & Yiping Wang & Ajay Nair & Somnath Tagore & Igor Katsyv & André F. Rendeiro & Amit Dipak Amin & Denis Schapiro & Chris J. Frangieh & Adrienne M. Luom, 2021. "A molecular single-cell lung atlas of lethal COVID-19," Nature, Nature, vol. 595(7865), pages 114-119, July.
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