Cited by 532SARS-CoV-2 and COVID-19 ResearchCOVID-19 Clinical Research StudiesPluripotent Stem Cells Research

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Identification of SARS-CoV-2 inhibitors using lung and colonic organoids

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Han, Yuling, Duan, Xiaohua, Yang, Liuliu, Nilsson-Payant, Benjamin E., Wang, Pengfei, Duan, Fuyu, Tang, Xuming, Yaron, Tomer M., Zhang, Tuo, Uhl, Skyler, Bram, Yaron, Richardson, Chanel, Zhu, Jiajun, Zhao, Zeping, Redmond, David, Houghton, Sean, Nguyen, Duc-Huy T., Xu, Dong, Wang, Xing, Jessurun, Jose, Borczuk, Alain, Huang, Yaoxing, Johnson, Jared L., Liu, Yuru, Xiang, Jenny, Wang, Hui, Cantley, Lewis C., tenOever, Benjamin R., Ho, David D., Pan, Fong Cheng, Evans, Todd, Chen, Huanhuan Joyce, Schwartz, Robert E., Chen, Shuibing·2021·Nature

DOI 10.1038/s41586-020-2901-9PMC PMC8034380

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Abstract

There is an urgent need to create novel models using human disease-relevant cells to study severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) biology and to facilitate drug screening. Here, as SARS-CoV-2 primarily infects the respiratory tract, we developed a lung organoid model using human pluripotent stem cells (hPSC-LOs). The hPSC-LOs (particularly alveolar type-II-like cells) are permissive to SARS-CoV-2 infection, and showed robust induction of chemokines following SARS-CoV-2 infection, similar to what is seen in patients with COVID-19. Nearly 25% of these patients also have gastrointestinal manifestations, which are associated with worse COVID-19 outcomes 1. We therefore also generated complementary hPSC-derived colonic organoids (hPSC-COs) to explore the response of colonic cells to SARS-CoV-2 infection. We found that multiple colonic cell types, especially enterocytes, express ACE2 and are permissive to SARS-CoV-2 infection. Using hPSC-LOs, we performed a high-throughput screen of drugs approved by the FDA (US Food and Drug Administration) and identified entry inhibitors of SARS-CoV-2, including imatinib, mycophenolic acid and quinacrine dihydrochloride. Treatment at physiologically relevant levels of these drugs significantly inhibited SARS-CoV-2 infection of both hPSC-LOs and hPSC-COs. Together, these data demonstrate that hPSC-LOs and hPSC-COs infected by SARS-CoV-2 can serve as disease models to study SARS-CoV-2 infection and provide a valuable resource for drug screening to identify candidate COVID-19 therapeutics.

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Authors: Han, Y., Duan, X., Yang, L., Nilsson-Payant, B. E., Wang, P., Duan, F., Tang, X., Yaron, T. M., Zhang, T., Uhl, S., Bram, Y., Richardson, C., Zhu, J., Zhao, Z., Redmond, D., Houghton, S., Nguyen, D.-H. T., Xu, D., Wang, X., Jessurun, J., Borczuk, A., Huang, Y., Johnson, J. L., Liu, Y., Xiang, J., Wang, H., Cantley, L. C., tenOever, B. R., Ho, D. D., Pan, F. C., Evans, T., Chen, H. J., Schwartz, R. E., & Chen, S.
Affiliations: Weill Cornell Medicine (US)
Shanghai Jiao Tong University (CN)
Icahn School of Medicine at Mount Sinai (US)
Aaron Diamond AIDS Research Center (US)
University of Chicago (US)
University of Illinois Chicago (US)
Corresponding author: Wang, Hui
Cantley, Lewis C.
tenOever, Benjamin R.
Ho, David D.
Pan, Fong Cheng
Evans, Todd
Chen, Huanhuan Joyce
Schwartz, Robert E.
Chen, Shuibing
ORCID: Han, Yuling
Duan, Xiaohua
Yang, Liuliu
Nilsson-Payant, Benjamin E.
Wang, Pengfei
Duan, Fuyu
Tang, Xuming
Yaron, Tomer M.
Zhang, Tuo
Uhl, Skyler
Bram, Yaron
Zhu, Jiajun
Redmond, David
Houghton, Sean
Nguyen, Duc-Huy T.
Xu, Dong
Wang, Xing
Jessurun, Jose
Borczuk, Alain
Huang, Yaoxing
Johnson, Jared L.
Liu, Yuru
Xiang, Jenny
Wang, Hui
Cantley, Lewis C.
tenOever, Benjamin R.
Ho, David D.
Pan, Fong Cheng
Evans, Todd
Chen, Huanhuan Joyce
Schwartz, Robert E.
Chen, Shuibing
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2020-10-28
Volume: 589
Issue: 7841
Pages: 270-275
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-020-2901-9
PMC: PMC8034380
OpenAlex: W3096177766
Cited by: 530
References: 33
Citations by year: 2026: 35 · 2025: 51 · 2024: 67 · 2023: 94 · 2022: 120 · 2021: 155 · 2020: 7
FWCI: 12.35
Type: journal article
Language: en
Update notices: correction (2024-05-29)
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: American Diabetes Association (7-20-COVID-211)
Icahn School of Medicine at Mount Sinai
Nature
National Institutes of Health
Defense Advanced Research Projects Agency (W911NF‐16‐C‐0050)
Weill Cornell Medical College
Advanced Research Projects Agency
National Cancer Institute (R00CA226353, R01CA234614)
National Institute of Allergy and Infectious Diseases (R01AI107301)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK124463, R01DK116075, R01DK119667, 1RO3DK117252, R01DK121072, DP3DK111907, R03DK117252)
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, COVID-19 pandemic, lung organoids, colonic organoids, human pluripotent stem cells, alveolar type II cells, enterocytes, ACE2 expression, entry inhibitors, imatinib, mycophenolic acid, high-throughput drug screening, FDA-approved drugs, antiviral activity, chemokine induction, gastrointestinal manifestations of COVID-19
MeSH terms: COVID-19, SARS-CoV-2, COVID-19 Drug Treatment, Animals, Antiviral Agents, Colon, Drug Evaluation, Preclinical, Female, Humans, Lung, Male, Organoids, United States, United States Food and Drug Administration, Drug Approval, Mice, Virus Internalization, Viral Tropism, Heterografts, In Vitro Techniques

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