Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions

Abstract Understanding how genes influence drug responses is critical for advancing personalized cancer treatments. However, identifying these gene-drug interactions in a physiologically relevant human system remains a challenge, as it requires a model that reflects the complexity and heterogeneity...

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Main Authors: Yuan-Hung Lo, Hudson T. Horn, Mo-Fan Huang, Wei-Chieh Yu, Chia-Mei Young, Qing Liu, Madeline Tomaske, Martina Towers, Antonia Dominguez, Michael C. Bassik, Dung-Fang Lee, Lei S. Qi, Jonathan S. Weissman, Jin Chen, Calvin J. Kuo
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62818-3
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author Yuan-Hung Lo
Hudson T. Horn
Mo-Fan Huang
Wei-Chieh Yu
Chia-Mei Young
Qing Liu
Madeline Tomaske
Martina Towers
Antonia Dominguez
Michael C. Bassik
Dung-Fang Lee
Lei S. Qi
Jonathan S. Weissman
Jin Chen
Calvin J. Kuo
author_facet Yuan-Hung Lo
Hudson T. Horn
Mo-Fan Huang
Wei-Chieh Yu
Chia-Mei Young
Qing Liu
Madeline Tomaske
Martina Towers
Antonia Dominguez
Michael C. Bassik
Dung-Fang Lee
Lei S. Qi
Jonathan S. Weissman
Jin Chen
Calvin J. Kuo
author_sort Yuan-Hung Lo
collection DOAJ
description Abstract Understanding how genes influence drug responses is critical for advancing personalized cancer treatments. However, identifying these gene-drug interactions in a physiologically relevant human system remains a challenge, as it requires a model that reflects the complexity and heterogeneity among individuals. Here we show that large-scale CRISPR-based genetic screens, including knockout, interference (CRISPRi), activation (CRISPRa), and single-cell approaches, can be applied in primary human 3D gastric organoids to systematically identify genes that affect sensitivity to cisplatin. Our screens uncover genes that modulate cisplatin response. By combining CRISPR perturbations with single-cell transcriptomics, we resolve how genetic alterations interact with cisplatin at the level of individual cells and uncover an unexpected link between fucosylation and cisplatin sensitivity. We identify TAF6L as a regulator of cell recovery from cisplatin-induced cytotoxicity. These results highlight the utility of human organoid models for dissecting gene-drug interactions and offer insights into therapeutic vulnerabilities in gastric cancer.
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spelling doaj-art-ad51621edbb941b9a5cd8674f0233f0f2025-08-20T03:46:25ZengNature PortfolioNature Communications2041-17232025-08-0116111810.1038/s41467-025-62818-3Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactionsYuan-Hung Lo0Hudson T. Horn1Mo-Fan Huang2Wei-Chieh Yu3Chia-Mei Young4Qing Liu5Madeline Tomaske6Martina Towers7Antonia Dominguez8Michael C. Bassik9Dung-Fang Lee10Lei S. Qi11Jonathan S. Weissman12Jin Chen13Calvin J. Kuo14Department of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer CenterDivision of Hematology, Department of Medicine, Stanford University School of MedicineThe University of Texas MD Anderson Cancer Center, UTHealth Houston Graduate School of Biomedical SciencesDepartment of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer CenterDepartment of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer CenterDepartment of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer CenterDivision of Hematology, Department of Medicine, Stanford University School of MedicineDepartment of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer CenterDepartment of Bioengineering, Stanford UniversityDepartment of Genetics, Stanford University School of MedicineThe University of Texas MD Anderson Cancer Center, UTHealth Houston Graduate School of Biomedical SciencesDepartment of Bioengineering, Stanford UniversityDepartment of Cellular and Molecular Pharmacology, University of CaliforniaLaboratory of Functional Genomics and Translational Control, Cecil H. and Ida Green Center for Reproductive Biology Sciences, University of Texas Southwestern Medical CenterDivision of Hematology, Department of Medicine, Stanford University School of MedicineAbstract Understanding how genes influence drug responses is critical for advancing personalized cancer treatments. However, identifying these gene-drug interactions in a physiologically relevant human system remains a challenge, as it requires a model that reflects the complexity and heterogeneity among individuals. Here we show that large-scale CRISPR-based genetic screens, including knockout, interference (CRISPRi), activation (CRISPRa), and single-cell approaches, can be applied in primary human 3D gastric organoids to systematically identify genes that affect sensitivity to cisplatin. Our screens uncover genes that modulate cisplatin response. By combining CRISPR perturbations with single-cell transcriptomics, we resolve how genetic alterations interact with cisplatin at the level of individual cells and uncover an unexpected link between fucosylation and cisplatin sensitivity. We identify TAF6L as a regulator of cell recovery from cisplatin-induced cytotoxicity. These results highlight the utility of human organoid models for dissecting gene-drug interactions and offer insights into therapeutic vulnerabilities in gastric cancer.https://doi.org/10.1038/s41467-025-62818-3
spellingShingle Yuan-Hung Lo
Hudson T. Horn
Mo-Fan Huang
Wei-Chieh Yu
Chia-Mei Young
Qing Liu
Madeline Tomaske
Martina Towers
Antonia Dominguez
Michael C. Bassik
Dung-Fang Lee
Lei S. Qi
Jonathan S. Weissman
Jin Chen
Calvin J. Kuo
Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
Nature Communications
title Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
title_full Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
title_fullStr Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
title_full_unstemmed Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
title_short Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions
title_sort large scale crispr screening in primary human 3d gastric organoids enables comprehensive dissection of gene drug interactions
url https://doi.org/10.1038/s41467-025-62818-3
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