SARS-CoV-2 Receptor ACE2 Is an Interferon-Stimulated Gene in Human Airway Epithelial Cells and Is Detected in Specific Cell Subsets across Tissues
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There is pressing urgency to understand the pathogenesis of the severe acute respiratory syndrome coronavirus clade 2 (SARS-CoV-2), which causes the disease COVID-19. SARS-CoV-2 spike (S) protein binds angiotensin-converting enzyme 2 (ACE2), and in concert with host proteases, principally transmembrane serine protease 2 (TMPRSS2), promotes cellular entry. The cell subsets targeted by SARS-CoV-2 in host tissues and the factors that regulate ACE2 expression remain unknown. Here, we leverage human, non-human primate, and mouse single-cell RNA-sequencing (scRNA-seq) datasets across health and disease to uncover putative targets of SARS-CoV-2 among tissue-resident cell subsets. We identify ACE2 and TMPRSS2 co-expressing cells within lung type II pneumocytes, ileal absorptive enterocytes, and nasal goblet secretory cells. Strikingly, we discovered that ACE2 is a human interferon-stimulated gene (ISG) in vitro using airway epithelial cells and extend our findings to in vivo viral infections. Our data suggest that SARS-CoV-2 could exploit species-specific interferon-driven upregulation of ACE2, a tissue-protective mediator during lung injury, to enhance infection.
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Co-expression of ACE2 and TMPRSS2 in nasal goblet secretory cells, lung type II pneumocytes, and ileal absorptive enterocytes is conserved in non-human primates and mice.
“A second study from the HCA Lung Biological Network extended the initial findings to tissues from non-human primates and mice, indicating co-expression of ACE2 and TMPRSS2 within nasal goblet secretory cells, lung type II pneumocytes, and ileal absorptive enterocytes (Ziegler et al., 2020).”
From COVID-19 and the human innate immune system (2021) · cites this paper as Ziegler et al., 2020
Inflammation can induce expression of ACE2 in human cells.
“Finally, it has recently been reported that inflammation can induce expression of ACE2 in human cells (87, 88). It is therefore possible that our survey of ACE2 expression, and other recent reports demonstrating expression of ACE2 in OE support and stem cells but not neurons (81, 89, 90), might under-represent the cell types that express ACE2 under conditions of CoV-2 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 [87]
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Self-citationDysregulation of type I interferon responses in COVID-19
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COVID-19 vaccines: The status and perspectives in delivery points of view
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Local and systemic responses to SARS-CoV-2 infection in children and adults
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Self-citationAnosmia in COVID-19: Underlying Mechanisms and Assessment of an Olfactory Route to Brain Infection
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Three-dimensional human alveolar stem cell culture models reveal infection response to SARS-CoV-2
Youk, J., Kim, T., Evans, K. V., Jeong, Y.-I., Hur, Y., Hong, S. P., Kim, J. H., Yi, K., Kim, S. Y., Na, K. J., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.10.004 · Cited by 266 · see citing works
Two distinct immunopathological profiles in autopsy lungs of COVID-19
Nienhold, R., Ciani, Y., Koelzer, V. H., Tzankov, A., Haslbauer, J. D., Menter, T., Schwab, N., Henkel, M., Frank, A., Zsikla, V., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18854-2 · Cited by 246 · see citing works
Adverse effects of COVID-19 mRNA vaccines: the spike hypothesis
Trougakos, I. P., Terpos, E., Alexopoulos, H., Politou, M., Paraskevis, D., Scorilas, A., Kastritis, E., Andreakos, E., & Dimopoulos, M. A. (2022) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2022.04.007 · Cited by 273 · see citing works
Onabajo, O. O., Banday, A. R., Stanifer, M. L., Yan, W., Obajemu, A., Santer, D. M., Florez-Vargas, O., Piontkivska, H., Vargas, J. M., Ring, T. J., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-00731-9 · Cited by 261 · see citing works
Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection
Desai, N., Neyaz, A., Szabolcs, A., Shih, A. R., Chen, J. H., Thapar, V., Nieman, L. T., Solovyov, A., Mehta, A., Lieb, D. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-20139-7 · Cited by 245 · see citing works
Impact of the Human Cell Atlas on medicine
Rood, J. E., Maartens, A., Hupalowska, A., Teichmann, S. A., & Regev, A. (2022) · Nature Medicine · doi:10.1038/s41591-022-02104-7 · Cited by 222 · see citing works
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Cheemarla, N. R., Watkins, T. A., Mihaylova, V. T., Wang, B., Zhao, D., Wang, G., Landry, M. L., & Foxman, E. F. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20210583 · Cited by 213 · see citing works
Leukocyte trafficking to the lungs and beyond: lessons from influenza for COVID-19
Alon, R., Sportiello, M., Kozlovski, S., Kumar, A., Reilly, E. C., Zarbock, A., Garbi, N., & Topham, D. J. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-020-00470-2 · Cited by 197 · see citing works
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COVID‐19 is an emergent disease of aging
Santesmasses, D., Castro, J. P., Zenin, A. A., Shindyapina, A. V., Gerashchenko, M. V., Zhang, B., Kerepesi, C., Yim, S. H., Fedichev, P. O., & Gladyshev, V. N. (2020) · Aging Cell · doi:10.1111/acel.13230 · Cited by 172 · see citing works
Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology
Ribeiro, D. E., Oliveira-Giacomelli, Á., Glaser, T., Arnaud-Sampaio, V. F., Andrejew, R., Dieckmann, L., Baranova, J., Lameu, C., Ratajczak, M. Z., & Ulrich, H. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00965-3 · Cited by 145 · see citing works
Ashary, N., Bhide, A., Chakraborty, P., Colaco, S., Mishra, A., Chhabria, K., Jolly, M. K., & Modi, D. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00783 · Cited by 121 · see citing works
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Baricitinib in hospitalised patients with COVID-19: a meta-analysis of randomised controlled trials
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COVID-19: neonatal–perinatal perspectives
On behalf of the Harvard Neonatal-Perinatal Fellowship COVID-19 Working Group, Barrero-Castillero, A., Beam, K. S., Bernardini, L. B., Ramos, E. G. C., Davenport, P. E., Duncan, A. R., Fraiman, Y. S., Frazer, L. C., Healy, H., et al. (2021) · Journal of Perinatology · doi:10.1038/s41372-020-00874-x · Cited by 92 · see citing works
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APOE interacts with ACE2 inhibiting SARS-CoV-2 cellular entry and inflammation in COVID-19 patients
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Immunological defense of CNS barriers against infections
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DNA damage response at telomeres boosts the transcription of SARS‐CoV‐2 receptor ACE2 during aging
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- Authors
- Ziegler, C. G. K., Allon, S. J., Nyquist, S. K., Mbano, I. M., Miao, V. N., Tzouanas, C. N., Cao, Y., Yousif, A. S., Bals, J., Hauser, B. M., Feldman, J., Muus, C., Wadsworth, M. H., Kazer, S. W., Hughes, T. K., Doran, B., Gatter, G. J., Vukovic, M., Taliaferro, F., Mead, B. E., Guo, Z., Wang, J. P., Gras, D., Plaisant, M., Ansari, M., Angelidis, I., Adler, H., Sucre, J. M. S., Taylor, C. J., Lin, B., Waghray, A., Mitsialis, V., Dwyer, D. F., Buchheit, K. M., Boyce, J. A., Barrett, N. A., Laidlaw, T. M., Carroll, S. L., Colonna, L., Tkachev, V., Peterson, C. W., Yu, A., Zheng, H. B., Gideon, H. P., Winchell, C. G., Lin, P. L., Bingle, C. D., Snapper, S. B., Kropski, J. A., Theis, F. J., Schiller, H. B., Zaragosi, L.-E., Barbry, P., Leslie, A., Kiem, H.-P., Flynn, J. L., Fortune, S. M., Berger, B., Finberg, R. W., Kean, L. S., Garber, M., Schmidt, A. G., Lingwood, D., Shalek, A. K., Ordovas-Montanes, J., Banovich, N., Barbry, P., Brazma, A., Desai, T., Duong, T. E., Eickelberg, O., Falk, C., Farzan, M., Glass, I., Haniffa, M., Horvath, P., Hung, D., Kaminski, N., Krasnow, M., Kropski, J. A., Kuhnemund, M., Lafyatis, R., Lee, H., Leroy, S., Linnarson, S., Lundeberg, J., Meyer, K., Misharin, A., Nawijn, M., Nikolic, M. Z., Ordovas-Montanes, J., Pe’er, D., Powell, J., Quake, S., Rajagopal, J., Tata, P. R., Rawlins, E. L., Regev, A., Reyfman, P. A., Rojas, M., Rosen, O., Saeb-Parsy, K., Samakovlis, C., Schiller, H., Schultze, J. L., Seibold, M. A., Shalek, A. K., Shepherd, D., Spence, J., Spira, A., Sun, X., Teichmann, S., Theis, F., Tsankov, A., van den Berge, M., von Papen, M., Whitsett, J., Xavier, R., Xu, Y., Zaragosi, L.-E., & Zhang, K.
- Affiliations
- Broad Institute (US)
- Africa Health Research Institute (ZA)
- University of Massachusetts Chan Medical School (US)
- Ragon Institute of MGH, MIT and Harvard (US)
- Harvard University (US)
- Inserm (FR)
- Centre National de la Recherche Scientifique (FR)
- Helmholtz Munich (DE)
- Vanderbilt University Medical Center (US)
- Massachusetts General Hospital (US)
- Brigham and Women's Hospital (US)
- University of California, Berkeley (US)
- University of Washington (US)
- Boston Children's Hospital (US)
- Seattle Children's Hospital (US)
- University of Pittsburgh (US)
- University of Sheffield (GB)
- MIT Computer Science and Artificial Intelligence Laboratory (US)
- ORCID
- Ziegler, Carly G.K.
- Allon, Samuel J.
- Nyquist, Sarah K.
- Mbano, Ian M.
- Miao, Vincent N.
- Tzouanas, Constantine N.
- Cao, Yuming
- Yousif, Ashraf S.
- Bals, Julia
- Hauser, Blake M.
- Feldman, Jared
- Muus, Christoph
- Wadsworth, Marc H.
- Kazer, Samuel W.
- Hughes, Travis K.
- Doran, Benjamin
- Gatter, G. James
- Mead, Benjamin E.
- Guo, Zhiru
- Wang, Jennifer P.
- Gras, Delphine
- Plaisant, Magali
- Ansari, Meshal
- Angelidis, Ilias
- Adler, Heiko
- Sucre, Jennifer M.S.
- Taylor, Chase J.
- Lin, Brian
- Waghray, Avinash
- Mitsialis, Vanessa
- Dwyer, Daniel F.
- Buchheit, Kathleen M.
- Boyce, Joshua A.
- Barrett, Nora A.
- Laidlaw, Tanya M.
- Carroll, Shaina L.
- Colonna, Lucrezia
- Tkachev, Victor
- Yu, Alison
- Zheng, Hengqi Betty
- Gideon, Hannah P.
- Winchell, Caylin G.
- Lin, Philana Ling
- Bingle, Colin D.
- Snapper, Scott B.
- Theis, Fabian J.
- Leslie, Alasdair
- Kiem, Hans-Peter
- Flynn, JoAnne L.
- Fortune, Sarah M.
- Berger, Bonnie
- Finberg, Robert W.
- Kean, Leslie S.
- Garber, Manuel
- Schmidt, Aaron G.
- Lingwood, Daniel
- Banovich, Nicholas
- Desai, Tushar
- Falk, Christine
- Farzan, Michael
- Glass, Ian
- Haniffa, Muzlifah
- Hung, Deborah
- Kaminski, Naftali
- Krasnow, Mark
- Lafyatis, Robert
- Leroy, Sylvie
- Lundeberg, Joakim
- Misharin, Alexander
- Nawijn, Martijn
- Pe’er, Dana
- Powell, Joseph
- Quake, Stephen
- Tata, Purushothama Rao
- Rawlins, Emma L.
- Regev, Aviv
- Reyfman, Paul A.
- Rojas, Mauricio
- Samakovlis, Christos
- Schultze, Joachim L.
- Seibold, Max A.
- Shepherd, Douglas
- Spence, Jason
- Spira, Avrum
- Sun, Xin
- Teichmann, Sarah
- Tsankov, Alexander
- Whitsett, Jeffrey
- Xavier, Ramnik
- Xu, Yan
- Zhang, Kun
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-05
- Volume
- 181
- Issue
- 5
- Pages
- 1016-1035.e19
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7252096
- OpenAlex
- W3011134208
- Cited by
- 2,284
- References
- 159
- Citations by year
- 2026: 50 · 2025: 93 · 2024: 172 · 2023: 233 · 2022: 425 · 2021: 730 · 2020: 578 · 2019: 3
- FWCI
- 64.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- eScholarship@UMassChan (submittedVersion, cc-by-nc-nd)
- HAL (submittedVersion, other-oa)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- UCL Discovery (University College London) (submittedVersion)
- Site cant be reached (submittedVersion, cc-by-nc-nd)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion, cc-by-nc-nd)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Apollo
- Funders
- National Institute of Allergy and Infectious Diseases (UM1 AI126623)
- Fondation pour la Recherche Médicale (DEQ20180339158)
- National Heart, Lung, and Blood Institute (U19 HL129902, DHHS/NIH 1UM1AI126617, U19 AI117945, R01 HL095791 NIH/NIAID R33-AI116184)
- Hertz Foundation (T32GM007753)
- Searle Scholars Program
- Richard and Susan Smith Family Foundation
- Bristol-Myers Squibb
- National Institute of General Medical Sciences
- Takeda Pharmaceuticals U.S.A.
- GlaxoSmithKline (DP2DA042422, 1R01HL128241-01, K23AI139352, R01AI124378, R01AI137057)
- Agence Nationale de la Recherche (U19 AI051731, ANR-19-CE14-0027)
- Bill and Melinda Gates Foundation (R56 AI139053)
- Massachusetts Institute of Technology
- National Science Foundation (1122374)
- Damon Runyon Cancer Research Foundation (DRG-2274-16)
- National Institutes of Health (5U24AI118672)
- 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 › Immunology and Microbiology › Immunology › interferon and immune responses
- Keywords
- SARS-CoV-2, ACE2, interferon-stimulated genes, interferon signaling, airway epithelial cells, TMPRSS2, viral entry, enterocytes, single-cell transcriptomics, COVID-19 pathogenesis, viral tropism
- MeSH terms
- Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, Adolescent, Animals, Cell Line, Cells, Cultured, Child, Humans, Influenza, Human, Interferon Type I, Peptidyl-Dipeptidase A, Lung, Macaca mulatta, Mycobacterium tuberculosis, Nasal Mucosa, Pneumonia, Viral, Receptors, Virus, Serine Endopeptidases, Tuberculosis, HIV Infections, Up-Regulation, Coronavirus Infections, Goblet Cells, Enterocytes, Mice, Alveolar Epithelial Cells, Pandemics, Single-Cell Analysis
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