Cited by 906SARS-CoV-2 and COVID-19 ResearchCOVID-19 Clinical Research Studiesinterferon and immune responses

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SARS-CoV-2 infection of human ACE2-transgenic mice causes severe lung inflammation and impaired function

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Winkler, Emma S., Bailey, Adam L., Kafai, Natasha M., Nair, Sharmila, McCune, Broc T., Yu, Jinsheng, Fox, Julie M., Chen, Rita E., Earnest, James T., Keeler, Shamus P., Ritter, Jon H., Kang, Liang-I, Dort, Sarah, Robichaud, Annette, Head, Richard, Holtzman, Michael J., Diamond, Michael S.·2020·Nature Immunology

DOI 10.1038/s41590-020-0778-2PMC PMC7578095

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Abstract

Although animal models have been evaluated for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, none have fully recapitulated the lung disease phenotypes seen in humans who have been hospitalized. Here, we evaluate transgenic mice expressing the human angiotensin I-converting enzyme 2 (ACE2) receptor driven by the cytokeratin-18 (K18) gene promoter (K18-hACE2) as a model of SARS-CoV-2 infection. Intranasal inoculation of SARS-CoV-2 in K18-hACE2 mice results in high levels of viral infection in lungs, with spread to other organs. A decline in pulmonary function occurs 4 days after peak viral titer and correlates with infiltration of monocytes, neutrophils and activated T cells. SARS-CoV-2-infected lung tissues show a massively upregulated innate immune response with signatures of nuclear factor-κB-dependent, type I and II interferon signaling, and leukocyte activation pathways. Thus, the K18-hACE2 model of SARS-CoV-2 infection shares many features of severe COVID-19 infection and can be used to define the basis of lung disease and test immune and antiviral-based countermeasures.

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LY6E protects mice from pathogenic effects of murine coronavirus and SARS-CoV-2Preprint
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InfluentialSelf-citation
Mild SARS-CoV-2 maternal infection in mice induces transient offspring neurodevelopmental aberrance
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Influential
Exploring coronavirus cell entry with functional viromics
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Immune Cells Are Differentially Affected by SARS-CoV-2 Viral Loads in K18-hACE2 Mice
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Characterization of the Pathogenic Features of Multiple SARS‐CoV‐2 Pandemic Strains in Different Mouse Models
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Background
Monitoring Group Activity of Hamsters and Mice as a Novel Tool to Evaluate COVID-19 Progression, Convalescence, and rVSV-ΔG-Spike Vaccination Efficacy
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Angiotensin-converting enzyme 2: virus accomplice or host defender?
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“[25,26] Consistent with previous reports, [27] we analyzed the RNA sequencing results in a published article [28] and found that glucose metabolism was promoted in mouse lung tissue infected with SARS-CoV-2 (Fig.”
Result
Unveiling Acacia farnesiana phytochemicals as Angiotensin Converting Enzyme (ACE) inhibitors via in-silico drug design, molecular docking, and bioavailability predictions: An illustration against SARS-CoV-2 spike protein
Rani, S., Madhumitha, B., Beelagi, M. S., Indrabalan, U. B., Mamathashree, M. N., Chandrashekar, S., Sk, K., Hemadri, D., Patil, S. S., & Suresh, K. (2022) · Journal of Ayurvedic and Herbal Medicine · doi:10.31254/jahm.2022.8401 · Cited by 1
“ACE2 is a zinc-containing type I membrane enzyme found on the surface of endothelial cells in the lungs, as well as other cell types and organs resulting in damage, inflammation, and respiratory distress [14,11] .”
Background
A Trans-Complementation System for SARS-CoV-2Preprint
Zhang, X., Liu, Y., Liu, J., Bailey, A. L., Plante, K. S., Plante, J. A., Zou, J., Xia, H., Bopp, N., Aguilar, P., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3770930 · Cited by 1
Self-citation
Neural epidermal growth factor-like 1 protein variant increases survival and modulates the inflammatory and immune responses in human ACE-2 transgenic mice infected with SARS-CoV-2Preprint
Biswas, R., Eaker, S. S., Soni, D. K., Kar, S., LoBato, D. N., & Culiat, C. T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.08.430254 · Cited by 1
“8 X 10(4) pfu), but resulted in the same rapid weight loss, behavioral and mortality phenotypes; hence, this treatment regimen is sufficient for generating clinically relevant disease features in hACE2 tg mice.(45) This pilot study was designed to examine if NV1 treatment of SARS-CoV-2 infected hACE2 mice increased su…”
BackgroundMethodResultInfluential
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Sheward, D. J., Mandolesi, M., Urgard, E., Kim, C., Hanke, L., Vidakovics, L. P., Pankow, A. P., Smith, N. L., Dopico, X. C., McInerney, G. M., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.03.438330 · Cited by 1
A broadly neutralizing biparatopic Nanobody protects mice from lethal challenge with SARS-CoV-2 variants of concernPreprint
Wagner, T. R., Schnepf, D., Beer, J., Klingel, K., Ruétalo, N., Kaiser, P. D., Junker, D., Sauter, M., Traenkle, B., Frecot, D. I., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.08.455562 · Cited by 1
Lung-selective Cas13d-based nanotherapy inhibits lethal SARS-CoV-2 infection by targeting host protease CtslPreprint
Cui, Z., Zeng, C., Huang, F., Yuan, F., Yan, J., Zhao, Y., Huang, J., Staats, H. F., Everitt, J. I., Sempowski, G. D., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.03.462915 · Cited by 1
Nasal prevention of SARS-CoV-2 infection by intranasal influenza-based boost vaccinationPreprint
Zhou, R., Wang, P., Wong, Y.-C., Xu, H., Lau, S.-Y., Liu, L., Mok, B. W.-Y., Peng, Q., Liu, N., Woo, K. F., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.21.465252 · Cited by 1
A third vaccination with a single T cell epitope protects against SARS-CoV-2 infection in the absence of neutralizing antibodiesPreprint
Pardieck, I. N., van der Gracht, E. T. I., Veerkamp, D. M. B., Behr, F. M., van Duikeren, S., Beyrend, G., Rip, J., Nadafi, R., van der Sluis, T. C., Nejad, E. B., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.15.472838 · Cited by 1
In contrast to T H 2-biased approaches, T H 1 COVID-19 vaccines protect Syrian hamsters from severe disease in the absence of dexamethasone-treatable vaccine-associated enhanced respiratory pathologyPreprint
Ebenig, A., Muraleedharan, S., Kazmierski, J., Tödt, D., Auste, A., Anzaghe, M., Gömer, A., Postmus, D., Gogesch, P., Niles, M. A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.28.474359 · Cited by 1
“While transgenic K18-ACE2 are no doubt useful for studying protection by vaccines, antibodies or antivirals against an exaggerated generalized form of the disease (Winkler et al., 2020), the predictability of the CoV-receptor transgenic mouse model for disease course in human patients seems somewhat questionable, espe…”
Background
Adenosine A2A Receptor (A 2A R) agonists improve survival in K28-hACE2 mice following SARS CoV-2 infectionPreprint
Mann, B. J., Chhabra, P., Ma, M., Brovero, S. G., Jones, M., Linden, J. M., & Brayman, K. L. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.25.481997 · Cited by 1
Vectored Immunoprophylaxis and Treatment of SARS-CoV-2 InfectionPreprint
Tada, T., Dcosta, B. M., Minnee, J., & Landau, N. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.11.523649 · Cited by 1
SARS-CoV-2 infection leads to Tau pathological signature in neuronsPreprint
Primio, C. D., Quaranta, P., Mignanelli, M., Siano, G., Bimbati, M., Piazza, C. R., Spezia, P. G., Perrera, P., Basolo, F., Poma, A. M., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.17.541098 · Cited by 1
The assembly of neutrophil inflammasomes during COVID-19 is mediated by type I interferonsPreprint
Cabrera, L. E., Jokiranta, S. T., Mäki, S., Miettinen, S., Kant, R., Kareinen, L., Sironen, T. A., Pietilä, J.-P., Kantele, A., Kekäläinen, E., et al. (2023) · medRxiv · doi:10.1101/2023.09.07.23295190 · Cited by 1
Dissecting the ocular impact of SARS-CoV-2 variants: Analysis of eye globe and retina in animal modelsPreprint
da Silva, J. L., Kersten, V., Dati, L. M. M., Lins, B. B., Tozzeto-Mendoza, T. R., Rodrigues, D. D. R. F., Vianna-Barbosa, R. J., Lima, S. H., Boas, L. S. V., da Silva, A. D. S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.29.596469 · Cited by 1
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Fantin, R. F., Clark, J. J., Cohn, H., Jaiswal, D., Bozarth, B., Civljak, A., Rao, V., Lobo, I., Nardulli, J., Srivastava, K., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.15.602781 · Cited by 1
The K18-hACE2 mouse model of SARS-CoV-2 infection to illustrate the role and response of the vasculature in neurotropic viral infectionPreprint
Neck, S. D., Penrice-Randal, R., Neves, L. X., Seehusen, F., Sharma, P., Helminger, B., Kirby, A., Mega, D., Erdmann, M., Zanella, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.07.637145 · Cited by 1

Authors: Winkler, E. S., Bailey, A. L., Kafai, N. M., Nair, S., McCune, B. T., Yu, J., Fox, J. M., Chen, R. E., Earnest, J. T., Keeler, S. P., Ritter, J. H., Kang, L.-I., Dort, S., Robichaud, A., Head, R., Holtzman, M. J., & Diamond, M. S.
Affiliations: Washington University in St. Louis (US)
Corresponding author: Diamond, Michael S.
ORCID: Winkler, Emma S.
Bailey, Adam L.
Kafai, Natasha M.
Nair, Sharmila
McCune, Broc T.
Yu, Jinsheng
Fox, Julie M.
Chen, Rita E.
Earnest, James T.
Keeler, Shamus P.
Ritter, Jon H.
Kang, Liang-I
Head, Richard
Holtzman, Michael J.
Diamond, Michael S.
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2020-08-24
Volume: 21
Issue: 11
Pages: 1327-1335
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-020-0778-2
PMC: PMC7578095
OpenAlex: W3080378920
Cited by: 901
References: 56
Citations by year: 2026: 55 · 2025: 72 · 2024: 124 · 2023: 131 · 2022: 234 · 2021: 252 · 2020: 32
FWCI: 21.20
Type: journal article
Language: en
Update notices: correction (2020-09-02)
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (75N93019C00062, R01 AI127828, R01 AI130591, R35 HL145242, F32 AI138392)
United States Department of Defense | Defense Advanced Research Projects Agency (HR001117S0019)
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, COVID-19 pandemic, K18-hACE2 mice, animal model of COVID-19, lung inflammation, lung function decline, monocytes, neutrophils, T cell activation, innate immune response, interferon signaling, NF-κB signaling
MeSH terms: Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, Animals, Chlorocebus aethiops, Disease Models, Animal, Female, Humans, Immunity, Innate, Interferon Type I, Interferon-gamma, Peptidyl-Dipeptidase A, Leukocytes, Lymphocyte Activation, Male, Mice, Transgenic, Monocytes, Neutrophils, Pneumonia, Pneumonia, Viral, Promoter Regions, Genetic, T-Lymphocytes, Vero Cells, Virus Replication, NF-kappa B, Coronavirus Infections, Neutrophil Infiltration, Mice, Keratin-18, Pandemics

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SARS-CoV-2 infection of human ACE2-transgenic mice causes severe lung inflammation and impaired function

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