SARS-CoV-2 Reverse Genetics Reveals a Variable Infection Gradient in the Respiratory Tract
Open accessAbstract
The mode of acquisition and causes for the variable clinical spectrum of coronavirus disease 2019 (COVID-19) remain unknown. We utilized a reverse genetics system to generate a GFP reporter virus to explore severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pathogenesis and a luciferase reporter virus to demonstrate sera collected from SARS and COVID-19 patients exhibited limited cross-CoV neutralization. High-sensitivity RNA in situ mapping revealed the highest angiotensin-converting enzyme 2 (ACE2) expression in the nose with decreasing expression throughout the lower respiratory tract, paralleled by a striking gradient of SARS-CoV-2 infection in proximal (high) versus distal (low) pulmonary epithelial cultures. COVID-19 autopsied lung studies identified focal disease and, congruent with culture data, SARS-CoV-2-infected ciliated and type 2 pneumocyte cells in airway and alveolar regions, respectively. These findings highlight the nasal susceptibility to SARS-CoV-2 with likely subsequent aspiration-mediated virus seeding to the lung in SARS-CoV-2 pathogenesis. These reagents provide a foundation for investigations into virus-host interactions in protective immunity, host susceptibility, and virus pathogenesis.
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In animal models of other coronaviruses and prior inactivated RSV or measles vaccines, VAERD is usually linked to Th2-biased CD4+ responses with elevated IL-4, IL-5, or IL-13.
“In animal models of infections with other coronaviruses and for previous whole-cell inactivated vaccines developed for respiratory syncytial virus and measles virus, VAERD has usually been associated with the development of T helper 2 cell (TH2 cell)-biased CD4+ T cell responses, with significantly increased levels of interleukin-4 (IL-4), IL-5 and/or IL-13 (refs12,126,165–174).”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [166]
Because CoV-2 can infect cells in the lower respiratory tract, the finding that human olfactory epithelium sustentacular cells express ACE2 at levels similar to the non-nasal respiratory tract is consistent with the possibility that these cells express ACE2 at a level permissive for direct infection.
“As CoV-2 can infect cells in the lower respiratory tract (40, 45), these results are consistent with the possibility that specific cell types in the human olfactory epithelium express ACE2 at a level that is permissive for direct infection.”
From Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia (2020) · cites this paper as [40]
Cells from the human upper airway, including nasal respiratory epithelium goblet and ciliated cells, express high levels of ACE2 and TMPRSS2, suggesting these respiratory epithelium cell types may serve as a viral reservoir during CoV-2 infection.
“It has recently been demonstrated through single cell RNA sequencing analysis (referred to herein as scSeq) that cells from the human upper airway — including nasal RE goblet and ciliated cells —express high levels of ACE2 and TMPRSS2, suggesting that these RE cell types may serve as a viral reservoir during CoV-2 infection (39, 40).”
From Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia (2020) · cites this paper as [40]
Recent findings in respiratory epithelium suggest scSeq substantially underestimates the fraction of a given cell type that expresses the Ace2 transcript, but new Ace2-expressing cell types are not discovered with more sensitive forms of analysis.
“These observations are consistent with recent findings in the respiratory epithelium suggesting that scSeq substantially underestimates the fraction of a given cell type that expresses the Ace2 transcript, but that “new” Ace2-expressing cell types are not discovered with more sensitive forms of analysis (40).”
From Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia (2020) · cites this paper as [40]
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Flagged first, then by citations
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- Authors
- Hou, Y. J., Okuda, K., Edwards, C. E., Martinez, D. R., Asakura, T., Dinnon, K. H., Kato, T., Lee, R. E., Yount, B. L., Mascenik, T. M., Chen, G., Olivier, K. N., Ghio, A., Tse, L. V., Leist, S. R., Gralinski, L. E., Schäfer, A., Dang, H., Gilmore, R., Nakano, S., Sun, L., Fulcher, M. L., Livraghi-Butrico, A., Nicely, N. I., Cameron, M., Cameron, C., Kelvin, D. J., de Silva, A., Margolis, D. M., Markmann, A., Bartelt, L., Zumwalt, R., Martinez, F. J., Salvatore, S. P., Borczuk, A., Tata, P. R., Sontake, V., Kimple, A., Jaspers, I., O’Neal, W. K., Randell, S. H., Boucher, R. C., & Baric, R. S.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- National Institutes of Health (US)
- Environmental Protection Agency (US)
- Case Western Reserve University (US)
- Dalhousie University (CA)
- University of New Mexico (US)
- Cornell University (US)
- Duke University (US)
- Corresponding author
- Boucher, Richard C.
- Baric, Ralph S.
- ORCID
- Hou, Yixuan J.
- Okuda, Kenichi
- Edwards, Caitlin E.
- Martinez, David R.
- Asakura, Takanori
- Dinnon, Kenneth H.
- Kato, Takafumi
- Lee, Rhianna E.
- Yount, Boyd L.
- Mascenik, Teresa M.
- Olivier, Kenneth N.
- Ghio, Andrew
- Tse, Longping V.
- Leist, Sarah R.
- Gralinski, Lisa E.
- Schäfer, Alexandra
- Dang, Hong
- Gilmore, Rodney
- Nakano, Satoko
- Sun, Ling
- Livraghi-Butrico, Alessandra
- Nicely, Nathan I.
- Cameron, Mark
- Cameron, Cheryl
- Kelvin, David J.
- Margolis, David M.
- Markmann, Alena
- Bartelt, Luther
- Salvatore, Steven P.
- Borczuk, Alain
- Tata, Purushothama R.
- Sontake, Vishwaraj
- Kimple, Adam
- Jaspers, Ilona
- O’Neal, Wanda K.
- Randell, Scott H.
- Boucher, Richard C.
- Baric, Ralph S.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-07
- Volume
- 182
- Issue
- 2
- Pages
- 429-446.e14
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7250779
- OpenAlex
- W3030748957
- Cited by
- 1,488
- References
- 101
- Citations by year
- 2026: 55 · 2025: 99 · 2024: 150 · 2023: 214 · 2022: 316 · 2021: 442 · 2020: 208 · 2019: 1 · 2018: 2
- FWCI
- 38.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNM’s Digital Repository (University of New Mexico) (submittedVersion)
- UNC Libraries
- Funders
- National Institute of Allergy and Infectious Diseases
- National Heart, Lung, and Blood Institute
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- SARS-CoV-2, COVID-19 pathogenesis, respiratory tract, ACE2 expression, aspiration, viral pathogenesis, cross-neutralization, alveolar epithelial cells, ciliated cells, airway epithelium, lung pathology
- MeSH terms
- Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, COVID-19 Serotherapy, Aged, Animals, Antibodies, Monoclonal, Cell Line, Cells, Cultured, Chlorocebus aethiops, Cystic Fibrosis, DNA, Recombinant, Female, Humans, Immunization, Passive, Peptidyl-Dipeptidase A, Lung, Male, Middle Aged, Nasal Mucosa, Pneumonia, Viral, Respiratory System, Serine Endopeptidases, Vero Cells, Virulence, Virus Replication, Coronavirus Infections, Furin, Antibodies, Neutralizing, Pandemics, Reverse Genetics
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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