Identification of SARS-CoV-2 inhibitors using lung and colonic organoids
Open accessAbstract
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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Screening over 1,000 FDA-approved drugs in colonic and lung organoids found SARS-CoV-2 entry inhibitors including imatinib, mycophenolic acid and quinacrine dihydrochloride.
“high-throughput screens of ≥1,000 drugs approved by the FDA run on colonic and lung organoids identified several SARS-CoV-2 entry inhibitors such as imatinib, mycophenolic acid and quinacrine dihydrochloride111.”
From Human disease models in drug development (2023) · cites this paper as [111]
The “A hPSC-LOs-based anti-SARS-CoV-2 screen” section identifies imatinib, mycophenolic acid and quinacrine dihydrochloride as entry-inhibitor hits from an FDA-approved drug library. But the high-throughput screen used lung organoids only; colonic organoids were used for subsequent validation (“Drugs block SARS-CoV-2 infection”). Our copy does not give a library size confirming ≥1,000 drugs. (LLM, conf=0.90)
Experimental — accuracy not yet measuredClinical trials have begun for amodiaquine and imatinib.
“amodiaquine (for example, NCT04532931, NCT04502342)51 and imatinib111 (for example, NCT04394416) have entered clinical trials.”
From Human disease models in drug development (2023) · cites this paper as [111]
The citation to this paper is attached to imatinib, not amodiaquine. The ‘Drugs block SARS-CoV-2 infection’ section reports imatinib experiments in organoids and Vero cells, but our copy does not say that imatinib entered a clinical trial or mention NCT04394416 (searched: clinical trials and the trial identifier). (LLM, conf=0.76)
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Organoid Models for Infectious Disease
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Applications of human organoids in the personalized treatment for digestive diseases
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The Progress of Intestinal Epithelial Models from Cell Lines to Gut-On-Chip
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Lung organoids, useful tools for investigating epithelial repair after lung injury
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Microfluidic Organs-on-a-Chip for Modeling Human Infectious Diseases
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Self-citationEndothelial contribution to COVID-19: an update on mechanisms and therapeutic implications
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Self-citationSARS-CoV-2 infects human adult donor eyes and hESC-derived ocular epithelium
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SARS-CoV-2 Infection of Airway Epithelial Cells
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Self-citationModular basis for potent SARS-CoV-2 neutralization by a prevalent VH1-2-derived antibody class
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Self-citationCoagulation factors directly cleave SARS-CoV-2 spike and enhance viral entry
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Self-citationAdvances in Microfluidic Technologies in Organoid Research
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Pathophysiology of infection with SARS‐CoV ‐2— What is known and what remains a mystery
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Self-citationRecent advances in human respiratory epithelium models for drug discovery
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Cardiomyocytes recruit monocytes upon SARS-CoV-2 infection by secreting CCL2
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Self-citationSARS-CoV-2 Infection and Lung Regeneration
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Machine Learning Models Identify Inhibitors of SARS-CoV-2
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Self-citationCommon Genetic Variation in Humans Impacts In Vitro Susceptibility to SARS-CoV-2 Infection
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Self-citationAdvanced lung organoids for respiratory system and pulmonary disease modeling
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Self-citationAlveolar Type II Cells and Pulmonary Surfactant in COVID-19 Era
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Artificial intelligence for drug repurposing against infectious diseases
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Advancing lung organoids for COVID-19 research
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Generation of Skin Organoids: Potential Opportunities and Challenges
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Organoid: a powerful tool to study lung regeneration and disease
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Applications of Brain Organoids for Infectious Diseases
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Merits and challenges of iPSC-derived organoids for clinical applications
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Organoids from pluripotent stem cells and human tissues: When two cultures meet each other
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Tailored Biosensors for Drug Screening, Efficacy Assessment, and Toxicity Evaluation
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Mechanisms of Lung Injury Induced by SARS-CoV-2 Infection
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Self-citationHuman Organoids and Organs‐on‐Chips for Addressing COVID‐19 Challenges
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Global Literature Analysis of Organoid and Organ‐on‐Chip Research
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Self-citationColloidal Aggregators in Biochemical SARS-CoV-2 Repurposing Screens
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Cross-validation of SARS-CoV-2 responses in kidney organoids and clinical populations
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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
- Published
- 2020-10-28
- Volume
- 589
- Issue
- 7841
- Pages
- 270-275
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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
- 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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