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Highly functional virus-specific cellular immune response in asymptomatic SARS-CoV-2 infection

View ORCID ProfileNina Le Bert, Hannah E Clapham, Anthony T Tan, Wan Ni Chia, Christine YL Tham, Jane M Lim, Kamini Kunasegaran, Linda Tan, Charles-Antoine Dutertre, Nivedita Shankar, Joey ME Lim, Louisa Jin Sun, Marina Zahari, Zaw Myo Tun, Vishakha Kumar, Beng Lee Lim, Siew Hoon Lim, Adeline Chia, Yee-Joo Tan, Paul Anantharajah Tambyah, Shirin Kalimuddin, David Lye, Jenny GH Low, Lin-Fa Wang, Wei Yee Wan, Li Yang Hsu, View ORCID ProfileAntonio Bertoletti, Clarence C Tam
doi: https://doi.org/10.1101/2020.11.25.399139
Nina Le Bert
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Hannah E Clapham
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Anthony T Tan
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Wan Ni Chia
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Christine YL Tham
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Jane M Lim
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Kamini Kunasegaran
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Linda Tan
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Charles-Antoine Dutertre
3Inserm U1015, Gustave Roussy, Villejuif, France
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Nivedita Shankar
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Joey ME Lim
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Louisa Jin Sun
4Infectious Diseases, Alexandra Hospital, National University Health System
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Marina Zahari
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Zaw Myo Tun
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Vishakha Kumar
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Beng Lee Lim
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Siew Hoon Lim
5Department of Microbiology, Singapore General Hospital, Singapore
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Adeline Chia
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Yee-Joo Tan
6Infectious Diseases Translational Programme, Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
7Institute of Molecular and Cell Biology, A*STAR, Singapore
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Paul Anantharajah Tambyah
8Infectious Disease, Department of Medicine, National University Hospital, Singapore
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Shirin Kalimuddin
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
9Department of Infectious Diseases, Singapore General Hospital, Singapore
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David Lye
10National Center of Infectious Diseases, Singapore
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Jenny GH Low
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
9Department of Infectious Diseases, Singapore General Hospital, Singapore
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Lin-Fa Wang
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Wei Yee Wan
5Department of Microbiology, Singapore General Hospital, Singapore
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Li Yang Hsu
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
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Antonio Bertoletti
1Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
11Singapore Immunology Network, A*STAR, Singapore
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  • For correspondence: antonio@duke-nus.edu.sg
Clarence C Tam
2Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore
12London School of Hygiene & Tropical Medicine, London, United Kingdom
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Abstract

The efficacy of virus-specific T cells in clearing pathogens involves a fine balance between their antiviral and inflammatory features. SARS-CoV-2-specific T cells in individuals who clear SARS-CoV-2 infection without symptoms or disease could reveal non-pathological yet protective characteristics. We therefore compared the quantity and function of SARS-CoV-2-specific T cells in a cohort of asymptomatic individuals (n=85) with that of symptomatic COVID-19 patients (n=76), at different time points after antibody seroconversion. We quantified T cells reactive to structural proteins (M, NP and Spike) using ELISpot assays, and measured the magnitude of cytokine secretion (IL-2, IFN-γ, IL-4, IL-6, IL-1β, TNF-α and IL-10) in whole blood following T cell activation with SARS-CoV-2 peptide pools as a functional readout. Frequencies of T cells specific for the different SARS-CoV-2 proteins in the early phases of recovery were similar between asymptomatic and symptomatic individuals. However, we detected an increased IFN-γ and IL-2 production in asymptomatic compared to symptomatic individuals after activation of SARS-CoV-2-specific T cells in blood. This was associated with a proportional secretion of IL-10 and pro-inflammatory cytokines (IL-6, TNF-α and IL-1β) only in asymptomatic infection, while a disproportionate secretion of inflammatory cytokines was triggered by SARS-CoV-2-specific T cell activation in symptomatic individuals. Thus, asymptomatic SARS-CoV-2 infected individuals are not characterized by a weak antiviral immunity; on the contrary, they mount a robust and highly functional virus-specific cellular immune response. Their ability to induce a proportionate production of IL-10 might help to reduce inflammatory events during viral clearance.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • One Sentence Summary: Virus-specific T cells secrete high levels of IFN-γ and IL-2 in asymptomatic SARS-CoV-2 infection.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 27, 2020.
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Highly functional virus-specific cellular immune response in asymptomatic SARS-CoV-2 infection
Nina Le Bert, Hannah E Clapham, Anthony T Tan, Wan Ni Chia, Christine YL Tham, Jane M Lim, Kamini Kunasegaran, Linda Tan, Charles-Antoine Dutertre, Nivedita Shankar, Joey ME Lim, Louisa Jin Sun, Marina Zahari, Zaw Myo Tun, Vishakha Kumar, Beng Lee Lim, Siew Hoon Lim, Adeline Chia, Yee-Joo Tan, Paul Anantharajah Tambyah, Shirin Kalimuddin, David Lye, Jenny GH Low, Lin-Fa Wang, Wei Yee Wan, Li Yang Hsu, Antonio Bertoletti, Clarence C Tam
bioRxiv 2020.11.25.399139; doi: https://doi.org/10.1101/2020.11.25.399139
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Highly functional virus-specific cellular immune response in asymptomatic SARS-CoV-2 infection
Nina Le Bert, Hannah E Clapham, Anthony T Tan, Wan Ni Chia, Christine YL Tham, Jane M Lim, Kamini Kunasegaran, Linda Tan, Charles-Antoine Dutertre, Nivedita Shankar, Joey ME Lim, Louisa Jin Sun, Marina Zahari, Zaw Myo Tun, Vishakha Kumar, Beng Lee Lim, Siew Hoon Lim, Adeline Chia, Yee-Joo Tan, Paul Anantharajah Tambyah, Shirin Kalimuddin, David Lye, Jenny GH Low, Lin-Fa Wang, Wei Yee Wan, Li Yang Hsu, Antonio Bertoletti, Clarence C Tam
bioRxiv 2020.11.25.399139; doi: https://doi.org/10.1101/2020.11.25.399139

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