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Combustible and electronic cigarette exposures increase ACE2 activity and SARS-CoV-2 Spike binding

Arunava Ghosh, Vishruth Girish, Monet Lou Yuan, Raymond D. Coakley, Neil E. Alexis, Erin L. Sausville, Anand Vasudevan, Alexander R. Chait, Jason M. Sheltzer, Robert Tarran
doi: https://doi.org/10.1101/2021.06.04.447156
Arunava Ghosh
1Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
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Vishruth Girish
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
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Monet Lou Yuan
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
3Johns Hopkins University, Baltimore, Maryland
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Raymond D. Coakley
4School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
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Neil E. Alexis
5Center for Environmental Medicine, Asthma and Lung Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
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Erin L. Sausville
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
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Anand Vasudevan
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
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Alexander R. Chait
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
6School of Medicine and Dentistry, University of Rochester, Rochester, New York
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Jason M. Sheltzer
2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
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  • For correspondence: sheltzer@cshl.edu robert_tarran@med.unc.edu
Robert Tarran
1Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina
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  • For correspondence: sheltzer@cshl.edu robert_tarran@med.unc.edu
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ABSTRACT

The outbreak of coronavirus disease 2019 (COVID-19) has extensively impacted global health. The causative pathogen, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), binds to the angiotensin-converting enzyme 2 (ACE2) receptor, a transmembrane metallo-carboxypeptidase that is expressed in both membrane-anchored (mACE2) and soluble (sACE2) forms in the lung. Tobacco use has been speculated as a vulnerability factor for contracting SARS-CoV-2 infection and subsequent disease severity, whilst electronic cigarettes (e-cigarettes) have been shown to induce harmful proteomic and immune changes in the lungs of vapers. We therefore tested the hypothesis that combustible tobacco (e.g. cigarettes) and non-combustible e-cigarettes could affect ACE2 activity and subsequent SARS-CoV-2 infection. We observed that sACE2 activity was significantly higher in bronchoalveolar lavage fluid from both smokers and vapers compared to age-matched non-smokers. Exposure to cigarette smoke increased ACE2 levels, mACE2 activity, and sACE2 in primary bronchial epithelial cultures. Finally, treatment with either cigarette smoke condensate or JUUL e-liquid increased infections with a spike-coated SARS-CoV-2 pseudovirus. Overall, these observations suggest that tobacco product use elevates ACE2 activity and increases the potential for SARS-CoV-2 infection through enhanced spike protein binding.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Co-first authors

  • FUNDING SOURCES: Funded by NIH/FDA HL120100, NIH/NHLBI HL135642, R01CA237652, 1DP5OD021385, NIH/FDA HL153698, an American Cancer Society Research Scholar Grant (to J.M.S.) and a New York Community Trust Grant (to J.M.S.).

  • DISCLAIMER: Research reported in this publication was supported in part by the National Institutes of Health (NIH) and the Family Smoking Prevention and Tobacco Control Act. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or the Food and Drug Administration.

  • CONFLICTS OF INTEREST: No conflicts of interest, financial or otherwise, are declared by the authors.

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 4.0 International license.
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Posted June 06, 2021.
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Combustible and electronic cigarette exposures increase ACE2 activity and SARS-CoV-2 Spike binding
Arunava Ghosh, Vishruth Girish, Monet Lou Yuan, Raymond D. Coakley, Neil E. Alexis, Erin L. Sausville, Anand Vasudevan, Alexander R. Chait, Jason M. Sheltzer, Robert Tarran
bioRxiv 2021.06.04.447156; doi: https://doi.org/10.1101/2021.06.04.447156
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Combustible and electronic cigarette exposures increase ACE2 activity and SARS-CoV-2 Spike binding
Arunava Ghosh, Vishruth Girish, Monet Lou Yuan, Raymond D. Coakley, Neil E. Alexis, Erin L. Sausville, Anand Vasudevan, Alexander R. Chait, Jason M. Sheltzer, Robert Tarran
bioRxiv 2021.06.04.447156; doi: https://doi.org/10.1101/2021.06.04.447156

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