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Multimodal characterization of antigen-specific CD8+ T cells across SARS-CoV-2 vaccination and infection

View ORCID ProfileBingjie Zhang, View ORCID ProfileRabi Upadhyay, View ORCID ProfileYuhan Hao, View ORCID ProfileMarie I. Samanovic, View ORCID ProfileRamin S. Herati, View ORCID ProfileJohn Blair, View ORCID ProfileJordan Axelrad, View ORCID ProfileMark J. Mulligan, View ORCID ProfileDan R. Littman, View ORCID ProfileRahul Satija
doi: https://doi.org/10.1101/2023.01.24.525203
Bingjie Zhang
1New York Genome Center, New York, NY, USA
2Center for Genomics and Systems Biology, New York University, New York, NY, USA
3Department of Cell Biology and Regenerative Medicine, New York University Grossman School of Medicine, New York, NY, USA
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Rabi Upadhyay
3Department of Cell Biology and Regenerative Medicine, New York University Grossman School of Medicine, New York, NY, USA
4Perlmutter Cancer Center, New York University Langone Health, New York, NY, USA
5Department of Medicine, New York University Grossman School of Medicine, New York, NY, USA
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Yuhan Hao
1New York Genome Center, New York, NY, USA
2Center for Genomics and Systems Biology, New York University, New York, NY, USA
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Marie I. Samanovic
5Department of Medicine, New York University Grossman School of Medicine, New York, NY, USA
6New York University Langone Vaccine Center, New York, NY, USA
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Ramin S. Herati
5Department of Medicine, New York University Grossman School of Medicine, New York, NY, USA
6New York University Langone Vaccine Center, New York, NY, USA
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John Blair
1New York Genome Center, New York, NY, USA
2Center for Genomics and Systems Biology, New York University, New York, NY, USA
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Jordan Axelrad
5Department of Medicine, New York University Grossman School of Medicine, New York, NY, USA
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Mark J. Mulligan
5Department of Medicine, New York University Grossman School of Medicine, New York, NY, USA
6New York University Langone Vaccine Center, New York, NY, USA
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Dan R. Littman
3Department of Cell Biology and Regenerative Medicine, New York University Grossman School of Medicine, New York, NY, USA
4Perlmutter Cancer Center, New York University Langone Health, New York, NY, USA
7Howard Hughes Medical Institute, New York, NY, USA
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  • For correspondence: rsatija@nygenome.org dan.littman@med.nyu.edu
Rahul Satija
1New York Genome Center, New York, NY, USA
2Center for Genomics and Systems Biology, New York University, New York, NY, USA
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  • For correspondence: rsatija@nygenome.org dan.littman@med.nyu.edu
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ABSTRACT

The human immune response to SARS-CoV-2 antigen after infection or vaccination is defined by the durable production of antibodies and T cells. Population-based monitoring typically focuses on antibody titer, but there is a need for improved characterization and quantification of T cell responses. Here, we utilize multimodal sequencing technologies to perform a longitudinal analysis of circulating human leukocytes collected before and after BNT162b2 immunization. Our data reveal distinct subpopulations of CD8+ T cells which reliably appear 28 days after prime vaccination (7 days post boost). Using a suite of cross-modality integration tools, we define their transcriptome, accessible chromatin landscape, and immunophenotype, and identify unique biomarkers within each modality. By leveraging DNA-oligo-tagged peptide-MHC multimers and T cell receptor sequencing, we demonstrate that this vaccine-induced population is SARS-CoV-2 antigen-specific and capable of rapid clonal expansion. Moreover, we also identify these CD8+ populations in scRNA-seq datasets from COVID-19 patients and find that their relative frequency and differentiation outcomes are predictive of subsequent clinical outcomes. Our work contributes to our understanding of T cell immunity, and highlights the potential for integrative and multimodal analysis to characterize rare cell populations.

Competing Interest Statement

In the past three years, R.S. has worked as a consultant for Bristol-Myers Squibb, Regeneron, and Kallyope and served as an SAB member for ImmunAI, Resolve Biosciences, Nanostring, and the NYC Pandemic Response Lab. D.R.L. is cofounder of Vedanta Biosciences and ImmunAI, on the advisory boards of IMIDomics and Evommune, and on the board of directors of Pfizer. MJM reported potential competing interests: laboratory research and clinical trials contracts with Lilly, Pfizer (exclusive of the current work), and Sanofi for vaccines or MAB vs SARS-CoV-2; contract funding from USG/HHS/BARDA for research specimen characterization and repository; research grant funding from USG/HHS/NIH for SARS-CoV-2 vaccine and MAB clinical trials; personal fees from Meissa Vaccines, Inc. and Pfizer for Scientific Advisory Board service. RSH has received research support from CareDx for SARS-CoV-2 vaccine studies. RSH is a consultant for Bristol-Myers-Squibb. All other authors declare no competing interests.

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 January 24, 2023.
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Multimodal characterization of antigen-specific CD8+ T cells across SARS-CoV-2 vaccination and infection
Bingjie Zhang, Rabi Upadhyay, Yuhan Hao, Marie I. Samanovic, Ramin S. Herati, John Blair, Jordan Axelrad, Mark J. Mulligan, Dan R. Littman, Rahul Satija
bioRxiv 2023.01.24.525203; doi: https://doi.org/10.1101/2023.01.24.525203
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Multimodal characterization of antigen-specific CD8+ T cells across SARS-CoV-2 vaccination and infection
Bingjie Zhang, Rabi Upadhyay, Yuhan Hao, Marie I. Samanovic, Ramin S. Herati, John Blair, Jordan Axelrad, Mark J. Mulligan, Dan R. Littman, Rahul Satija
bioRxiv 2023.01.24.525203; doi: https://doi.org/10.1101/2023.01.24.525203

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