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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“Therefore, transgenic mouse models expressing the human ACE2 receptor driven by cytokeratin-18 (K18-hACE2) allowed the study of SARS-CoV-2 infection to recapitulate several aspects of lung inflammation observed in severe and non-severe COVID-19 manifestations [79,80].”
Vasculature-on-a-chip platform with innate immunity enables identification of angiopoietin-1 derived peptide as a therapeutic for SARS-CoV-2 induced inflammation
Lu, R. X. Z., Lai, B. F. L., Rafatian, N., Gustafson, D., Campbell, S. B., Banerjee, A., Kozak, R., Mossman, K., Mubareka, S., Howe, K. L., et al. (2022) · Lab on a Chip · doi:10.1039/d1lc00817j · Cited by 58
Ketogenic diet restrains aging-induced exacerbation of coronavirus infection in mice
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“…infection with mCoV-A59 is pneumotropic and causes ARDS in C57BL/6J animals, while all other MHV strains require the A/J or type-I interferon-deficient background, for the development of severe disease (De Albuquerque et al., 2006; Khanolkar et al., 2009; Yang et al., 2014) limiting their use.”
Background
Simvastatin Downregulates the SARS-CoV-2-Induced Inflammatory Response and Impairs Viral Infection Through Disruption of Lipid Rafts
Teixeira, L., Temerozo, J. R., Pereira-Dutra, F. S., Ferreira, A. C., Mattos, M., Gonçalves, B. S., Sacramento, C. Q., Palhinha, L., Cunha‐Fernandes, T., Dias, S. D. S. G., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.820131 · Cited by 55
Platelet activation by SARS-CoV-2 implicates the release of active tissue factor by infected cells
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Spike-Dependent Opsonization Indicates Both Dose-Dependent Inhibition of Phagocytosis and That Non-Neutralizing Antibodies Can Confer Protection to SARS-CoV-2
Bahnan, W., Wrighton, S., Sundwall, M., Bläckberg, A., Larsson, O. J., Höglund, U., Khakzad, H., Godzwon, M., Walle, M., Elder, E. E., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.808932 · Cited by 58
Mice infected with Mycobacterium tuberculosis are resistant to acute disease caused by secondary infection with SARS-CoV-2
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“CoV2 infection elicits the expression of multiple inflammatory genes in mouse lungs [12].”
BackgroundMethod
Preclinical evaluation of a SARS-CoV-2 mRNA vaccine PTX-COVID19-B
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Intranasal versus intratracheal exposure to lipopolysaccharides in a murine model of acute respiratory distress syndrome
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“SARS-CoV-2 infection of human ACE2-transgenic mice in which ACE2 expression is driven by the cytokeratin-18 promoter [55] also revealed a progressive inflammatory process starting at PID 2 in perivascular sites.”
Background
Multifunctional angiotensin converting enzyme 2, the SARS-CoV-2 entry receptor, and critical appraisal of its role in acute lung injury
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Post-exposure protection of SARS-CoV-2 lethal infected K18-hACE2 transgenic mice by neutralizing human monoclonal antibody
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A third vaccination with a single T cell epitope confers protection in a murine model of SARS-CoV-2 infection
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Bacterial-induced or passively administered interferon gamma conditions the lung for early control of SARS-CoV-2
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“2E) 47 . iv BCG protected K18-hACE2 mice against weight loss and resulted in lower viral loads, but no signi ﬁ cant protection was observed in animals treated with anti-IFN γ (Fig.”
SARS-CoV-2 infection in K18-ACE2 transgenic mice replicates human pulmonary disease in COVID-19
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Complete protection by a single-dose skin patch–delivered SARS-CoV-2 spike vaccine
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Neurotropic Effects of SARS-CoV-2 Modeled by the Human Brain Organoids
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“Human brain organoids are particularly instrumental formodelingCOVID-19 because rodents have significant limitations to faithfully recapitulate human COVID-19 symptoms as they require overexpression of human ACE2 to facilitate viral entry and to exhibit COVID-19 phenotypes (Hoffmann et al., 2020; Winkler et al., 2020;…”
Human-Based Advanced in vitro Approaches to Investigate Lung Fibrosis and Pulmonary Effects of COVID-19
Kiener, M., Roldán, N., Machahua, C., Sengupta, A., Geiser, T., Guenat, O. T., Funke-Chambour, M., Hobi, N., & Julio, M. K. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.644678 · Cited by 52
“Humanized ACE2 mice develop COVID-19 and pathologic tissue remodeling has been confirmed in their lungs ∼3 days post-infection (217, 219, 220).”
Background
Impaired immune response drives age-dependent severity of COVID-19
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Applications of Brain Organoids for Infectious Diseases
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“More importantly, some viruses do not infect mouse cells efficiently due to the lack of necessary cellular components, such as the ACE receptor, which is critical for SARS-CoV-2 infection.(22,23) Although mouse models have allowed us to learn a great deal about neurotropic viruses, it is also important to have human-d…”
Background
Cellular mechanisms underlying neurological/neuropsychiatric manifestations of COVID‐19
Bodnar, B. H., Patel, K., Ho, W., Luo, J. J., & Hu, W. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26720 · Cited by 51
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Self-citation
Mefloquine, a Potent Anti-severe Acute Respiratory Syndrome-Related Coronavirus 2 (SARS-CoV-2) Drug as an Entry Inhibitor in vitro
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SARS-CoV-2 variants of concern display enhanced intrinsic pathogenic properties and expanded organ tropism in mouse models
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Mechanisms of Lung Injury Induced by SARS-CoV-2 Infection
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Intranasal administration of BReC-CoV-2 COVID-19 vaccine protects K18-hACE2 mice against lethal SARS-CoV-2 challenge
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CVnCoV protects human ACE2 transgenic mice from ancestral B BavPat1 and emerging B.1.351 SARS-CoV-2
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Kidney Disease Modeling with Organoids and Organs-on-Chips
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A Biosafety Level 2 Mouse Model for Studying Betacoronavirus-Induced Acute Lung Damage and Systemic Manifestations
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Nasal prevention of SARS-CoV-2 infection by intranasal influenza-based boost vaccination in mouse models
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) · EBioMedicine · doi:10.1016/j.ebiom.2021.103762 · Cited by 50
Neutrophil-Dependent Immunity During Pulmonary Infections and Inflammations
Effah, C. Y., Drokow, E. K., Agboyibor, C., Ding, L., He, S., Liu, S., Akorli, S. Y., Nuamah, E., Sun, T., Zhou, X., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.689866 · Cited by 51
“Different cytokines produced by local airway cells (Thymic stromal lymphopoietin and IL-33, IL-25, IL-23, IL-17, IL-10, IL-1-b, IL-1-alpha), are those that transmit the relevant biological impact of chemokines.”
BackgroundMethodInfluential
SARS-CoV-2 activates the TLR4/MyD88 pathway in human macrophages: A possible correlation with strong pro-inflammatory responses in severe COVID-19
Sahanic, S., Hilbe, R., Dünser, C., Tymoszuk, P., Löffler‐Ragg, J., Rieder, D., Trajanoski, Z., Krogsdam, A., Demetz, E., Yurchenko, M., et al. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e21893 · Cited by 47
Interstitial macrophages are a focus of viral takeover and inflammation in COVID-19 initiation in human lung
Wu, T.-H., Travaglini, K. J., Rustagi, A., Xu, D., Zhang, Y., Andronov, L. P., Jang, S., Gillich, A., Dehghannasiri, R., Martínez-Colón, G. J., et al. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20232192 · Cited by 56
“…dangerous when they reach the alveoli (Bao et al., 2020; Jiang et al., 2020; Lamers and Haagmans, 2022; Munster et al., 2020; Rockx et al., 2020; Winkler et al., 2020), the site of gas exchange, but the critical transition to life-threatening pneumonia and acute respiratory distress syndrome…”
Background
SARS-CoV-2 aberrantly elevates mitochondrial bioenergetics to induce robust virus propagation
Shin, H. J., Lee, W., Ku, K. B., Yoon, G. Y., Moon, H.-W., Kim, C., Kim, M.-H., Yi, Y.-S., Jun, S., Kim, B., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01836-x · Cited by 52
“61,62 We observed that SARS-CoV-2-induced severe clinical symptoms are signi ﬁ cantly alleviated by vandetanib treatment (Fig.”
Background
The Bacterial Mucosal Immunotherapy MV130 Protects Against SARS-CoV-2 Infection and Improves COVID-19 Vaccines Immunogenicity
del Fresno, C., García‐Arriaza, J., Martínez-Cano, S., Heras‐Murillo, I., Jarit-Cabanillas, A., Amores-Iniesta, J., Brandi, P., Dunphy, G., Suay‐Corredera, C., Pricolo, M. R., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.748103 · Cited by 46
“Moreover, considering that acute SARS-CoV-2 infection is linked to leukopenia both in patients (23, 24) and in the K18hACE2 mouse model used in our study (13), MV130 could be generating and/or maintaining a beneficial pro-immunogenic airway environment, ready to respond to SARS-CoV-2, early upon infection.”
Method
Lyophilized, thermostable Spike or RBD immunogenic liposomes induce protective immunity against SARS-CoV-2 in mice
Mabrouk, M. T., Chiem, K., Rujas, E., Huang, W., Jahagirdar, D., Quinn, B., Nair, M. S., Nissly, R. H., Cavener, V. S., Boyle, N. R., et al. (2021) · Science Advances · doi:10.1126/sciadv.abj1476 · Cited by 47
Experimental Models of COVID-19
Caldera-Crespo, L. A., Paidas, M. J., Roy, S., Schulman, C. I., Kenyon, N. S., Daunert, S., & Jayakumar, A. R. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.792584 · Cited by 47
SARS-CoV-2 infection induces protective immunity and limits transmission in Syrian hamsters
Selvaraj, P., Lien, C. Z., Liu, S.-F., Stauft, C., Nuñez, I. A., Hernandez, M., Nimako, E., Ortega, M. A., Starost, M., Dennis, J., et al. (2021) · Life Science Alliance · doi:10.26508/lsa.202000886 · Cited by 47
“This ﬁ nding contrasts with the reported lethal encephalitis seen in a subset of infected K18-hACE2 mice (14 Preprint , 15, 16, 17).”
Intranasal gene therapy to prevent infection by SARS-CoV-2 variants
Sims, J. J., Greig, J. A., Michalson, K. T., Lian, S., Martino, R. A., Meggersee, R., Turner, K. B., Nambiar, K., Dyer, C., Hinderer, C. J., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009544 · Cited by 42
Interleukin-1RA Mitigates SARS-CoV-2–Induced Inflammatory Lung Vascular Leakage and Mortality in Humanized K18-hACE-2 Mice
Xiong, S., Zhang, L., Qadir, A. S., Richner, J. M., Class, J., Rehman, J., & Malik, A. B. (2021) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.121.316925 · Cited by 48
Domain-based mRNA vaccines encoding spike protein N-terminal and receptor binding domains confer protection against SARS-CoV-2
Stewart-Jones, G., Elbashir, S. M., Wu, K., Lee, D., Renzi, I., Ying, B., Koch, M., Sein, C. E., Choi, A., Whitener, B. M., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adf4100 · Cited by 55
Self-citation
Mucosal vaccine-induced cross-reactive CD8+ T cells protect against SARS-CoV-2 XBB.1.5 respiratory tract infection
Ying, B., Darling, T. L., Desai, P., Liang, C.-Y., Dmitriev, I. P., Soudani, N., Bricker, T. L., Kashentseva, E. A., Harastani, H., Raju, S., et al. (2024) · Nature Immunology · doi:10.1038/s41590-024-01743-x · Cited by 49
Self-citation
DNA origami presenting the receptor binding domain of SARS-CoV-2 elicit robust protective immune response
Oktay, E., Alem, F., Hernandez, K. R., Girgis, M. J., Green, C. M., Mathur, D., Medintz, I. L., Narayanan, A., & Veneziano, R. (2023) · Communications Biology · doi:10.1038/s42003-023-04689-2 · Cited by 47
Evolution of nasal and olfactory infection characteristics of SARS-CoV-2 variants
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Small-molecule inhibition of SARS-CoV-2 NSP14 RNA cap methyltransferase
Meyer, C., Garzia, A., Miller, M. W., Huggins, D. J., Myers, R. W., Hoffmann, H.-H., Ashbrook, A. W., Jannath, S. Y., Liverton, N. J., Kargman, S., et al. (2024) · Nature · doi:10.1038/s41586-024-08320-0 · Cited by 45
SARS-CoV-2 in animals: From potential hosts to animal models
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L-SIGN is a receptor on liver sinusoidal endothelial cells for SARS-CoV-2 virus
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A Novel Soluble ACE2 Protein Provides Lung and Kidney Protection in Mice Susceptible to Lethal SARS-CoV-2 Infection
Hassler, L., Wysocki, J. A., Gelarden, I. A., Sharma, I., Τοματσίδου, Α., Ye, M., Gula, H., Nicoleascu, V., Randall, G. C., Pshenychnyi, S., et al. (2022) · Journal of the American Society of Nephrology · doi:10.1681/asn.2021091209 · Cited by 44
Current Status of Putative Animal Sources of SARS-CoV-2 Infection in Humans: Wildlife, Domestic Animals and Pets
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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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