IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39096-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39096-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39096-y?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. 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. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    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. Cai He & Jingyun Yang & Weiqi Hong & Zimin Chen & Dandan Peng & Hong Lei & Aqu Alu & Xuemei He & Zhenfei Bi & Xiaohua Jiang & Guowen Jia & Yun Yang & Yanan Zhou & Wenhai Yu & Cong Tang & Qing Huang & , 2022. "A self-assembled trimeric protein vaccine induces protective immunity against Omicron variant," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Yubin Liu & Ziyi Wang & Xinyu Zhuang & Shengnan Zhang & Zhicheng Chen & Yan Zou & Jie Sheng & Tianpeng Li & Wanbo Tai & Jinfang Yu & Yanqun Wang & Zhaoyong Zhang & Yunfeng Chen & Liangqin Tong & Xi Yu, 2023. "Inactivated vaccine-elicited potent antibodies can broadly neutralize SARS-CoV-2 circulating variants," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Taha Y. Taha & Irene P. Chen & Jennifer M. Hayashi & Takako Tabata & Keith Walcott & Gabriella R. Kimmerly & Abdullah M. Syed & Alison Ciling & Rahul K. Suryawanshi & Hannah S. Martin & Bryan H. Bach , 2023. "Rapid assembly of SARS-CoV-2 genomes reveals attenuation of the Omicron BA.1 variant through NSP6," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Yin-Feng Kang & Cong Sun & Jing Sun & Chu Xie & Zhen Zhuang & Hui-Qin Xu & Zheng Liu & Yi-Hao Liu & Sui Peng & Run-Yu Yuan & Jin-Cun Zhao & Mu-Sheng Zeng, 2022. "Quadrivalent mosaic HexaPro-bearing nanoparticle vaccine protects against infection of SARS-CoV-2 variants," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Tomohiro Takano & Takashi Sato & Ryutaro Kotaki & Saya Moriyama & Shuetsu Fukushi & Masahiro Shinoda & Kiyomi Kabasawa & Nagashige Shimada & Mio Kousaka & Yu Adachi & Taishi Onodera & Kazutaka Terahar, 2023. "Heterologous SARS-CoV-2 spike protein booster elicits durable and broad antibody responses against the receptor-binding domain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Alief Moulana & Thomas Dupic & Angela M. Phillips & Jeffrey Chang & Serafina Nieves & Anne A. Roffler & Allison J. Greaney & Tyler N. Starr & Jesse D. Bloom & Michael M. Desai, 2022. "Compensatory epistasis maintains ACE2 affinity in SARS-CoV-2 Omicron BA.1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Laura Heydemann & Małgorzata Ciurkiewicz & Georg Beythien & Kathrin Becker & Klaus Schughart & Stephanie Stanelle-Bertram & Berfin Schaumburg & Nancy Mounogou-Kouassi & Sebastian Beck & Martin Zickler, 2023. "Hamster model for post-COVID-19 alveolar regeneration offers an opportunity to understand post-acute sequelae of SARS-CoV-2," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Kuei-Pin Chung & Chih-Ning Cheng & Yi-Jung Chen & Chia-Lang Hsu & Yen-Lin Huang & Min-Shu Hsieh & Han-Chun Kuo & Ya-Ting Lin & Yi-Hsiu Juan & Kiichi Nakahira & Yen-Fu Chen & Wei-Lun Liu & Sheng-Yuan R, 2024. "Alveolar epithelial cells mitigate neutrophilic inflammation in lung injury through regulating mitochondrial fatty acid oxidation," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    9. Zhennan Zhao & Jingya Zhou & Mingxiong Tian & Min Huang & Sheng Liu & Yufeng Xie & Pu Han & Chongzhi Bai & Pengcheng Han & Anqi Zheng & Lutang Fu & Yuanzhu Gao & Qi Peng & Ying Li & Yan Chai & Zengyua, 2022. "Omicron SARS-CoV-2 mutations stabilize spike up-RBD conformation and lead to a non-RBM-binding monoclonal antibody escape," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Maik Pietzner & Robert Lorenz Chua & Eleanor Wheeler & Katharina Jechow & Julian D. S. Willett & Helena Radbruch & Saskia Trump & Bettina Heidecker & Hugo Zeberg & Frank L. Heppner & Roland Eils & Mar, 2022. "ELF5 is a potential respiratory epithelial cell-specific risk gene for severe COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Praveen Weeratunga & Laura Denney & Joshua A. Bull & Emmanouela Repapi & Martin Sergeant & Rachel Etherington & Chaitanya Vuppussetty & Gareth D. H. Turner & Colin Clelland & Jeongmin Woo & Amy Cross , 2023. "Single cell spatial analysis reveals inflammatory foci of immature neutrophil and CD8 T cells in COVID-19 lungs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Shaofeng Deng & Ying Liu & Rachel Chun-Yee Tam & Pin Chen & Anna Jinxia Zhang & Bobo Wing-Yee Mok & Teng Long & Anja Kukic & Runhong Zhou & Haoran Xu & Wenjun Song & Jasper Fuk-Woo Chan & Kelvin Kai-W, 2023. "An intranasal influenza virus-vectored vaccine prevents SARS-CoV-2 replication in respiratory tissues of mice and hamsters," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Khadija Khan & Farina Karim & Yashica Ganga & Mallory Bernstein & Zesuliwe Jule & Kajal Reedoy & Sandile Cele & Gila Lustig & Daniel Amoako & Nicole Wolter & Natasha Samsunder & Aida Sivro & James Emm, 2022. "Omicron BA.4/BA.5 escape neutralizing immunity elicited by BA.1 infection," Nature Communications, Nature, vol. 13(1), pages 1-7, December.
    14. Urban Lendahl & Lars Muhl & Christer Betsholtz, 2022. "Identification, discrimination and heterogeneity of fibroblasts," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    15. Christina Beck & Deepak Ramanujam & Paula Vaccarello & Florenc Widenmeyer & Martin Feuerherd & Cho-Chin Cheng & Anton Bomhard & Tatiana Abikeeva & Julia Schädler & Jan-Peter Sperhake & Matthias Graw &, 2023. "Trimannose-coupled antimiR-21 for macrophage-targeted inhalation treatment of acute inflammatory lung damage," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    16. Pablo Jané & Xiaoying Xu & Vincent Taelman & Eduardo Jané & Karim Gariani & Rebecca A. Dumont & Yonathan Garama & Francisco Kim & María Val Gomez & Martin A. Walter, 2023. "The Imageable Genome," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Guoli Shi & Tiansheng Li & Kin Kui Lai & Reed F. Johnson & Jonathan W. Yewdell & Alex A. Compton, 2024. "Omicron Spike confers enhanced infectivity and interferon resistance to SARS-CoV-2 in human nasal tissue," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. Wenkai Han & Ningning Chen & Xinzhou Xu & Adil Sahil & Juexiao Zhou & Zhongxiao Li & Huawen Zhong & Elva Gao & Ruochi Zhang & Yu Wang & Shiwei Sun & Peter Pak-Hang Cheung & Xin Gao, 2023. "Predicting the antigenic evolution of SARS-COV-2 with deep learning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    19. Dhiraj K. Singh & Ekaterina Aladyeva & Shibali Das & Bindu Singh & Ekaterina Esaulova & Amanda Swain & Mushtaq Ahmed & Journey Cole & Chivonne Moodley & Smriti Mehra & Larry S. Schlesinger & Maxim N. , 2022. "Myeloid cell interferon responses correlate with clearance of SARS-CoV-2," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. Emanuele Andreano & Ida Paciello & Silvia Marchese & Lorena Donnici & Giulio Pierleoni & Giulia Piccini & Noemi Manganaro & Elisa Pantano & Valentina Abbiento & Piero Pileri & Linda Benincasa & Ginevr, 2022. "Anatomy of Omicron BA.1 and BA.2 neutralizing antibodies in COVID-19 mRNA vaccinees," Nature Communications, Nature, vol. 13(1), pages 1-8, 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_s41467-023-39096-y. 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.