Three-dimensional human alveolar stem cell culture models reveal infection response to SARS-CoV-2
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Abstract
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which is the cause of a present pandemic, infects human lung alveolar type 2 (hAT2) cells. Characterizing pathogenesis is crucial for developing vaccines and therapeutics. However, the lack of models mirroring the cellular physiology and pathology of hAT2 cells limits the study. Here, we develop a feeder-free, long-term, three-dimensional (3D) culture technique for hAT2 cells derived from primary human lung tissue and investigate infection response to SARS-CoV-2. By imaging-based analysis and single-cell transcriptome profiling, we reveal rapid viral replication and the increased expression of interferon-associated genes and proinflammatory genes in infected hAT2 cells, indicating a robust endogenous innate immune response. Further tracing of viral mutations acquired during transmission identifies full infection of individual cells effectively from a single viral entry. Our study provides deep insights into the pathogenesis of SARS-CoV-2 and the application of defined 3D hAT2 cultures as models for respiratory diseases.
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Alveolospheres have been instrumental in providing key insights into alveolar regeneration, epithelial-mesenchymal cross talk, and viral infections such as SARS-CoV-2.
“They have been particularly instrumental in providing key insights into alveolar regeneration, epithelial-mesenchymal cross talk and more recently of viral infections, e.g. SARS-CoV-2 (Katsura et al., 2020; Youk et al., 2020).”
From Pulmonary fibrosis: Emerging diagnostic and therapeutic strategies (2023) · cites this paper as Youk et al., 2020
Human alveolar organoids are derived from AEC2s.
“Human alveolar organoids are derived from AEC2s and depending on the culture conditions, AEC2s can give rise to organoids alone (Katsura et al., 2020; J. H. Kim et al., 2021; Youk et al., 2020), or require the presence of a mesenchymal feeder layer (Barkauskas et al., 2013), and can differentiate into alveolar epithelial type 1 (AEC1) cells.”
From Pulmonary fibrosis: Emerging diagnostic and therapeutic strategies (2023) · cites this paper as Youk et al., 2020
Depending on culture conditions, AEC2s can give rise to organoids alone.
“depending on the culture conditions, AEC2s can give rise to organoids alone (Katsura et al., 2020; J. H. Kim et al., 2021; Youk et al., 2020)”
From Pulmonary fibrosis: Emerging diagnostic and therapeutic strategies (2023) · cites this paper as Youk et al., 2020
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SARS-CoV-2 Research Using Human Pluripotent Stem Cells and Organoids
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Scientific Validation and Clinical Application of Lung Cancer Organoids
Lee, D., Kim, Y., & Chung, C. (2021) · Cells · doi:10.3390/cells10113012 · Cited by 25 · see citing works
Self-citationOrganoid Studies in COVID-19 Research
Kim, J., Koo, B., & Clevers, H. C. (2022) · International Journal of Stem Cells · doi:10.15283/ijsc21251 · Cited by 25 · see citing works
Self-citationThree-dimensional models of the lung: past, present and future: a mini review
Sen, C., Freund, D., & Gomperts, B. N. (2022) · Biochemical Society Transactions · doi:10.1042/bst20190569 · Cited by 23 · see citing works
Lung Organoids in Smoking Research: Current Advances and Future Promises
Agraval, H., & Chu, H. W. (2022) · Biomolecules · doi:10.3390/biom12101463 · Cited by 25 · see citing works
Chen, J., & Na, F. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1066869 · Cited by 25 · see citing works
Establishment of human distal lung organoids for SARS-CoV-2 infection
Wang, T., Zhang, N., Fan, S., Zhao, L., Song, W., Gong, Y., Shen, Q., Zhang, C., Ren, P., Lin, C., et al. (2021) · Cell Discovery · doi:10.1038/s41421-021-00346-2 · Cited by 24 · see citing works
Human stem cell‐based models for studying host‐pathogen interactions
Pellegrino, E., & Gutierrez, M. (2021) · Cellular Microbiology · doi:10.1111/cmi.13335 · Cited by 20 · see citing works
Dissecting single-cell genomes through the clonal organoid technique
Youk, J., Kwon, H. W., Kim, R., & Ju, Y. S. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00680-1 · Cited by 21 · see citing works
Self-citationWhen stem cells meet COVID-19: recent advances, challenges and future perspectives
Li, S., Zhu, H., Zhao, M., Liu, W., Wang, L., Zhu, B., Xie, W. J., Zhao, C., Zhou, Y., Ren, C., et al. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02683-1 · Cited by 21 · see citing works
Organoids: Principle, application and perspective
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Lim, K., Rutherford, E. N., Delpiano, L., He, P., Lin, W., Sun, D., van den Boomen, D. J. H., Edgar, J. R., Bang, J. H., Predeus, A. V., et al. (2025) · The EMBO Journal · doi:10.1038/s44318-024-00328-6 · Cited by 20 · see citing works
Self-citation3D-printed airway model as a platform for SARS-CoV-2 infection and antiviral drug testing
Lee, Y., Lee, M. K., Lee, H., Kim, B., Kim, M., & Jung, S. (2024) · Biomaterials · doi:10.1016/j.biomaterials.2024.122689 · Cited by 20 · see citing works
Gandikota, C., Vaddadi, K., Sivasami, P., Huang, C., Liang, Y., Pushparaj, S., Deng, X., Channappanavar, R., Metcalf, J. P., & Liu, L. (2024) · Journal of Medical Virology · doi:10.1002/jmv.29579 · Cited by 19 · see citing works
Choi, S., Choi, J., Cheon, S., Song, J., Kim, S.-Y., Kim, J.-E., Nam, D.-H., Manzar, G. S., Kim, S., Kang, H., et al. (2022) · Cell Biology and Toxicology · doi:10.1007/s10565-022-09698-1 · Cited by 19 · see citing works
Self-citationFRET-Based haCE2 Receptor Mimic Peptide Conjugated Nanoprobe for Simple Detection of SARS-CoV-2
Kang, B., Lee, Y., Lim, J., Yong, D., Choi, Y. K., Yoon, S. W., Seo, S., Jang, S., Son, S. U., Kang, T., et al. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.136143 · Cited by 20 · see citing works
Lung Organoids for Hazard Assessment of Nanomaterials
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Runft, S., Färber, I., Krüger, J., Krüger, N., Armando, F., Rocha, C., Pöhlmann, S., Burigk, L., Leitzen, E., Ciurkiewicz, M., et al. (2022) · Veterinary Pathology · doi:10.1177/03009858211073678 · Cited by 19 · see citing works
Three-Dimensional Cell Culture Models to Study Respiratory Virus Infections Including COVID-19
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Human lung organoid modelling of tissue-resident antiviral T cell responses
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A novelin vitrotubular model to recapitulate features of distal airways: the bronchioid
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Three-Dimensional Cell Cultures as a Research Platform in Lung Diseases and COVID-19
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Yoo, G., Park, D., Kim, Y., & Chung, C. (2021) · Cancers · doi:10.3390/cancers13123069 · Cited by 17 · see citing works
Self-citationTopical TMPRSS2 inhibition prevents SARS-CoV-2 infection in differentiated human airway cultures
Guo, W., Porter, L., Crozier, T. W. M., Coates, M. S., Jha, A., McKie, M. A., Nathan, J. A., Lehner, P. J., Greenwood, E. J. D., & McCaughan, F. (2022) · Life Science Alliance · doi:10.26508/lsa.202101116 · Cited by 17 · see citing works
Lung organoids in COPD: recent advances and future prospects
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- Authors
- 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., Bleazard, T., Kim, H. M., Fellows, M., Mahbubani, K. T., Saeb-Parsy, K., Kim, S. Y., Kim, Y. T., Koh, G. Y., Choi, B.-S., Ju, Y. S., & Lee, J.-H.
- Affiliations
- Korea Advanced Institute of Science and Technology (KR)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- Korea National Institute of Health (KR)
- Institute for Basic Science (KR)
- Seoul National University Hospital (KR)
- National Institute for Biological Standards and Control (GB)
- AstraZeneca (United Kingdom) (GB)
- University of Cambridge (GB)
- Corresponding author
- Kim, Young Tae
- Koh, Gou Young
- Choi, Byeong-Sun
- Ju, Young Seok
- Lee, Joo-Hyeon
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2020-12
- Volume
- 27
- Issue
- 6
- Pages
- 905-919.e10
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC7577700
- OpenAlex
- W3094609450
- Cited by
- 266
- References
- 92
- Citations by year
- 2026: 20 · 2025: 37 · 2024: 24 · 2023: 39 · 2022: 58 · 2021: 83 · 2020: 5
- FWCI
- 6.07
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- Apollo
- Funders
- Institute for Basic Science
- Royal Society
- Korea Health Industry Development Institute
- Biotechnology and Biological Sciences Research Council
- College of Medicine, Seoul National University
- Human Frontier Science Program
- European Research Council
- National Research Foundation of Korea
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- SARS-CoV-2, alveolar type II cells, 3D cell culture, feeder-free culture, lung stem cells, viral infection response, innate immune response, interferon genes, pro-inflammatory genes, viral replication, single-cell transcriptomics, viral mutations, COVID-19 pathogenesis
- MeSH terms
- COVID-19, SARS-CoV-2, Culture Media, Humans, Interferons, Models, Biological, Pulmonary Alveoli, Stem Cells, Virus Replication, Cell Culture Techniques, Virus Internalization, Transcriptome
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