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Single-cell analysis of upper airway cells reveals host-viral dynamics in influenza infected adults

View ORCID ProfileYuming Cao, Zhiru Guo, Pranitha Vangala, View ORCID ProfileElisa Donnard, Ping Liu, Patrick McDonel, Jose Ordovas-Montanes, Alex K. Shalek, Robert W. Finberg, Jennifer P. Wang, Manuel Garber
doi: https://doi.org/10.1101/2020.04.15.042978
Yuming Cao
1Department of Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA, USA
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  • ORCID record for Yuming Cao
Zhiru Guo
2Department of Medicine, University of Massachusetts Medical School, Worcester, MA, USA
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Pranitha Vangala
1Department of Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA, USA
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Elisa Donnard
1Department of Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA, USA
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  • ORCID record for Elisa Donnard
Ping Liu
2Department of Medicine, University of Massachusetts Medical School, Worcester, MA, USA
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Patrick McDonel
1Department of Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA, USA
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Jose Ordovas-Montanes
6Division of Gastroenterology Boston Children’s Hospital and Program in Immunology Harvard Medical School, Boston, MA, USA
7Harvard Stem Cell Institute, Cambridge, MA
8Broad Institute of MIT and Harvard, Cambridge, MA, USA
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Alex K. Shalek
4Institute for Medical Engineering and Science, Department of Chemistry & Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA, USA
5Ragon Institute of MGH, MIT and Harvard, Cambridge MA, USA
7Harvard Stem Cell Institute, Cambridge, MA
8Broad Institute of MIT and Harvard, Cambridge, MA, USA
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Robert W. Finberg
2Department of Medicine, University of Massachusetts Medical School, Worcester, MA, USA
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Jennifer P. Wang
2Department of Medicine, University of Massachusetts Medical School, Worcester, MA, USA
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Manuel Garber
1Department of Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA, USA
3Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA, USA
9Department of Dermatology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA
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  • For correspondence: manuel.garber@umassmed.edu
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Abstract

Influenza virus infections are major causes of morbidity and mortality. Research using cultured cells, bulk tissue, and animal models cannot fully capture human disease dynamics. Many aspects of virus-host interactions in a natural setting remain unclear, including the specific cell types that are infected and how they and neighboring bystander cells contribute to the overall antiviral response. To address these questions, we performed single-cell RNA sequencing (scRNA-Seq) on cells from freshly collected nasal washes from healthy human donors and donors diagnosed with acute influenza during the 2017-18 season. We describe a previously uncharacterized goblet cell population, specific to infected individuals, with high expression of MHC class II genes. Furthermore, leveraging scRNA-Seq reads, we obtained deep viral genome coverage and developed a model to rigorously identify infected cells that detected influenza infection in all epithelial cell types and even some immune cells. Our data revealed that each donor was infected by a unique influenza variant and that each variant was separated by at least one unique non-synonymous difference. Our results demonstrate the power of massively-parallel scRNA-Seq to study viral variation, as well as host and viral transcriptional activity during human infection.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Co-senior authors

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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-ND 4.0 International license.
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Posted April 17, 2020.
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Single-cell analysis of upper airway cells reveals host-viral dynamics in influenza infected adults
Yuming Cao, Zhiru Guo, Pranitha Vangala, Elisa Donnard, Ping Liu, Patrick McDonel, Jose Ordovas-Montanes, Alex K. Shalek, Robert W. Finberg, Jennifer P. Wang, Manuel Garber
bioRxiv 2020.04.15.042978; doi: https://doi.org/10.1101/2020.04.15.042978
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Single-cell analysis of upper airway cells reveals host-viral dynamics in influenza infected adults
Yuming Cao, Zhiru Guo, Pranitha Vangala, Elisa Donnard, Ping Liu, Patrick McDonel, Jose Ordovas-Montanes, Alex K. Shalek, Robert W. Finberg, Jennifer P. Wang, Manuel Garber
bioRxiv 2020.04.15.042978; doi: https://doi.org/10.1101/2020.04.15.042978

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