Progenitor identification and SARS-CoV-2 infection in human distal lung organoids
Open accessAbstract
The distal lung contains terminal bronchioles and alveoli that facilitate gas exchange. Three-dimensional in vitro human distal lung culture systems would strongly facilitate the investigation of pathologies such as interstitial lung disease, cancer and coronavirus disease 2019 (COVID-19) pneumonia caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Here we describe the development of a long-term feeder-free, chemically defined culture system for distal lung progenitors as organoids derived from single adult human alveolar epithelial type II (AT2) or KRT5+ basal cells. AT2 organoids were able to differentiate into AT1 cells, and basal cell organoids developed lumens lined with differentiated club and ciliated cells. Single-cell analysis of KRT5+ cells in basal organoids revealed a distinct population of ITGA6+ITGB4+ mitotic cells, whose offspring further segregated into a TNFRSF12A hi subfraction that comprised about ten per cent of KRT5+ basal cells. This subpopulation formed clusters within terminal bronchioles and exhibited enriched clonogenic organoid growth activity. We created distal lung organoids with apical-out polarity to present ACE2 on the exposed external surface, facilitating infection of AT2 and basal cultures with SARS-CoV-2 and identifying club cells as a target population. This long-term, feeder-free culture of human distal lung organoids, coupled with single-cell analysis, identifies functional heterogeneity among basal cells and establishes a facile in vitro organoid model of human distal lung infections, including COVID-19-associated pneumonia.
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Zang and colleagues used CRISPR-Cas9 and drug screenings to show that knockouts of TMPRSS2 or TMPRSS4, or treatment with Camostat, can reduce SARS-CoV-2 viral infection.
“Zang and colleagues used CRISPR-Cas9 and drug screenings to show that knock-outs of either TMPRSS2 or TMPRSS4, or treatment with Camostat can reduce viral infection184.”
From Organoids (2022) · cites this paper as [184]
The SARS-CoV-2 and H1N1 infection section reports infection of distal lung organoids and TMPRSS2 expression, but not TMPRSS2 or TMPRSS4 knockouts or Camostat treatment. The Extended Data passage describes antiviral screening for H1N1, not the claimed SARS-CoV-2 interventions. Searches for TMPRSS4, Camostat, CRISPR-Cas9, and Zang did not locate a passage supporting the claim in our copy. (LLM, conf=0.76)
Experimental — accuracy not yet measuredStudies in intestinal organoids show that SARS-CoV-2 can infect enterocytes.
“Studies in intestinal organoids show that SARS-Cov-2 can also infect enterocytes183,184.”
From Organoids (2022) · cites this paper as [184]
The ‘SARS-CoV-2 and H1N1 infection of organoids’ section reports infection in distal lung organoids, including AT2 and club cells, not intestinal organoids or enterocytes. Searches for intestinal organoids and gut enterocytes found no passage reporting the claimed finding; the References section lists a gut-enterocyte study but does not establish the intestinal-organoid claim in this paper’s text. (LLM, conf=0.75)
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- Authors
- Salahudeen, A. A., Choi, S. S., Rustagi, A., Zhu, J., van Unen, V., de la O, S. M., Flynn, R. A., Margalef-Català, M., Santos, A. J. M., Ju, J., Batish, A., Usui, T., Zheng, G. X. Y., Edwards, C. E., Wagar, L. E., Luca, V., Anchang, B., Nagendran, M., Nguyen, K., Hart, D. J., Terry, J. M., Belgrader, P., Ziraldo, S. B., Mikkelsen, T. S., Harbury, P. B., Glenn, J. S., Garcia, K. C., Davis, M. M., Baric, R. S., Sabatti, C., Amieva, M. R., Blish, C. A., Desai, T. J., & Kuo, C. J.
- Affiliations
- University of Illinois Chicago (US)
- Stanford Medicine (US)
- Stanford University (US)
- 10X Genomics (United States) (US)
- University of North Carolina at Chapel Hill (US)
- Howard Hughes Medical Institute (US)
- Chan Zuckerberg Biohub San Francisco (US)
- Corresponding author
- Blish, Catherine A.
- Desai, Tushar J.
- Kuo, Calvin J.
- ORCID
- Salahudeen, Ameen A.
- Choi, Shannon S.
- Rustagi, Arjun
- Zhu, Junjie
- van Unen, Vincent
- Flynn, Ryan A.
- Margalef-Català, Mar
- Santos, António J. M.
- Batish, Arpit
- Usui, Tatsuya
- Zheng, Grace X. Y.
- Edwards, Caitlin E.
- Wagar, Lisa E.
- Luca, Vincent
- Anchang, Benedict
- Hart, Daniel J.
- Mikkelsen, Tarjei S.
- Harbury, Pehr B.
- Glenn, Jeffrey S.
- Garcia, K. Christopher
- Davis, Mark M.
- Baric, Ralph S.
- Sabatti, Chiara
- Amieva, Manuel R.
- Blish, Catherine A.
- Desai, Tushar J.
- Kuo, Calvin J.
- Venue
- Nature
- Published
- 2020-11-25
- Volume
- 588
- Issue
- 7839
- Pages
- 670-675
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC8003326
- OpenAlex
- W3110287817
- Cited by
- 416
- References
- 50
- Citations by year
- 2026: 38 · 2025: 58 · 2024: 55 · 2023: 65 · 2022: 105 · 2021: 90 · 2020: 5
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- UNC Libraries
- Funders
- National Science Foundation (1712800)
- Howard Hughes Medical Institute
- Bill and Melinda Gates Foundation (OPP 1113682, U19AI057229)
- Damon Runyon Cancer Research Foundation (DRG-2286-17, 2286-17)
- American College of Radiology Imaging Network
- Wellcome Trust
- ECOG-ACRIN Cancer Research Group
- Novo Nordisk
- Novo Nordisk Fonden (NNF19OC0056411)
- National Institutes of Health (DK11572802, 1ug3hl145623-01, USA-WA1/2020)
- Centers for Disease Control and Prevention
- National Heart, Lung, and Blood Institute (R01HL142549)
- National Cancer Institute (U01CA176299, UH3CA255135, U01CA217851)
- National Institute of General Medical Sciences (T32GM007365)
- National Institute of Allergy and Infectious Diseases (R01AI157155, R56AI111460, U19AI057229, U19AI116484, T32AI007502)
- National Institute of Diabetes and Digestive and Kidney Diseases (U24DK085532, U01DK085527, U01DK085532)
- National Institute of Dental and Craniofacial Research (K08DE027730, U01DE025188)
- Stanford Cancer Institute
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
- Keywords
- COVID-19 pandemic, COVID-19 pneumonia, lung progenitor cells, alveolar type II cells, basal cells, keratin 5, Clara cells, ciliated cells, TNFRSF12A, ACE2, feeder-free culture, chemically defined culture, single-cell analysis, organoid culture
- MeSH terms
- TWEAK Receptor, COVID-19, SARS-CoV-2, Cell Differentiation, Cell Division, Clone Cells, Humans, Lung, Models, Biological, Organoids, Pneumonia, Viral, Integrin alpha6, Integrin beta4, Tissue Culture Techniques, Influenza A Virus, H1N1 Subtype, Keratin-5, Alveolar Epithelial Cells, Single-Cell Analysis, In Vitro Techniques
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