Cited by 1,082Cystic Fibrosis Research AdvancesNeonatal Respiratory Health ResearchTissue Engineering and Regenerative Medicine

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Long‐term expanding human airway organoids for disease modeling

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Sachs, Norman, Papaspyropoulos, Angelos, Zomer‐van Ommen, Domenique D, Heo, Inha, Böttinger, Lena, Klay, Dymph, Weeber, Fleur, Huelsz‐Prince, Guizela, Iakobachvili, Nino, Amatngalim, Gimano D, de Ligt, Joep, van Hoeck, Arne, Proost, Natalie, Viveen, Marco C, Lyubimova, Anna, Teeven, Luc, Derakhshan, Sepideh, Korving, Jeroen, Begthel, Harry, Dekkers, Johanna F, Kumawat, Kuldeep, Ramos, Emilio, van Oosterhout, Matthijs FM, Offerhaus, G Johan, Wiener, Dominique J, Olimpio, Eduardo P, Dijkstra, Krijn K, Smit, Egbert F, van der Linden, Maarten, Jaksani, Sridevi, van de Ven, Marieke, Jonkers, Jos, Rios, Anne C, Voest, Emile E, van Moorsel, Coline HM, van der Ent, Cornelis K, Cuppen, Edwin, van Oudenaarden, Alexander, Coenjaerts, Frank E, Meyaard, Linde, Bont, Louis J, Peters, Peter J, Tans, Sander J, van Zon, Jeroen S, Boj, Sylvia F, Vries, Robert G, Beekman, Jeffrey M, Clevers, Hans·2019·The EMBO Journal

DOI 10.15252/embj.2018100300PMC PMC6376275

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Abstract

Abstract Organoids are self-organizing 3D structures grown from stem cells that recapitulate essential aspects of organ structure and function. Here we describe a method to establish long-term-expanding human airway organoids from broncho-alveolar biopsies or lavage material. The pseudostratified airway organoid epithelium consists of basal cells, functional multi-ciliated cells, mucus-producing goblet cells, and CC10-secreting club cells. Airway organoids derived from cystic fibrosis (CF) patients allow assessment of CFTR function in an organoid swelling assay. Organoid culture conditions also allow gene editing as well as the derivation of various types of lung cancer organoids. Respiratory syncytial virus (RSV) infection recapitulated central disease features and dramatically increases organoid cell motility, found to be driven by the non-structural viral NS2 protein. We conclude that human airway organoids represent versatile models for the in vitro study of hereditary, malignant, and infectious pulmonary disease.

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Additional file 4 of Expression-based species deconvolution and realignment removes misalignment error in multispecies single-cell data
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Additional file 2 of Transcriptomic analysis of tumor tissues and organoids reveals the crucial genes regulating the proliferation of lung adenocarcinoma
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Additional file 2 of Mapping the scientific output of organoids for animal and human modeling infectious diseases: a bibliometric assessment
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Additional file 6 of Expression-based species deconvolution and realignment removes misalignment error in multispecies single-cell data
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Additional file 7 of Expression-based species deconvolution and realignment removes misalignment error in multispecies single-cell data
Choi, J., Lee, W., Yoon, J.-K., Choi, S. M., Lee, C.-H., Moon, H.-G., Cho, S., Chung, J.-H., Yang, H.-K., & Kim, J.-I. (2022) · Figshare · doi:10.6084/m9.figshare.19695762
Additional file 1 of Transcriptomic analysis of tumor tissues and organoids reveals the crucial genes regulating the proliferation of lung adenocarcinoma
Ma, X., Yang, S., Jiang, H., Wang, Y., & Xiang, Z. (2021) · Figshare · doi:10.6084/m9.figshare.16456203
Additional file 3 of Transcriptomic analysis of tumor tissues and organoids reveals the crucial genes regulating the proliferation of lung adenocarcinoma
Ma, X., Yang, S., Jiang, H., Wang, Y., & Xiang, Z. (2021) · Figshare · doi:10.6084/m9.figshare.16456212
Additional file 5 of Expression-based species deconvolution and realignment removes misalignment error in multispecies single-cell data
Choi, J., Lee, W., Yoon, J.-K., Choi, S. M., Lee, C.-H., Moon, H.-G., Cho, S., Chung, J.-H., Yang, H.-K., & Kim, J.-I. (2022) · Figshare · doi:10.6084/m9.figshare.19695756
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Preclinical Patient-Derived Tumor Organoids for Modeling Cancer
Somuncu, O. (2026) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-032-10024-5_1

Authors: Sachs, N., Papaspyropoulos, A., Zomer‐van Ommen, D. D., Heo, I., Böttinger, L., Klay, D., Weeber, F., Huelsz‐Prince, G., Iakobachvili, N., Amatngalim, G. D., de Ligt, J., van Hoeck, A., Proost, N., Viveen, M. C., Lyubimova, A., Teeven, L., Derakhshan, S., Korving, J., Begthel, H., Dekkers, J. F., Kumawat, K., Ramos, E., van Oosterhout, M. F., Offerhaus, G. J., Wiener, D. J., Olimpio, E. P., Dijkstra, K. K., Smit, E. F., van der Linden, M., Jaksani, S., van de Ven, M., Jonkers, J., Rios, A. C., Voest, E. E., van Moorsel, C. H., van der Ent, C. K., Cuppen, E., van Oudenaarden, A., Coenjaerts, F. E., Meyaard, L., Bont, L. J., Peters, P. J., Tans, S. J., van Zon, J. S., Boj, S. F., Vries, R. G., Beekman, J. M., & Clevers, H.
Affiliations: University Medical Center Utrecht (NL)
St. Antonius Ziekenhuis (NL)
The Netherlands Cancer Institute (NL)
Institute for Atomic and Molecular Physics (NL)
Maastricht University (NL)
Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
Princess Máxima Center (NL)
Royal Netherlands Academy of Arts and Sciences (NL)
Corresponding author: Clevers, Hans
ORCID: Sachs, Norman
Papaspyropoulos, Angelos
Klay, Dymph
Weeber, Fleur
Iakobachvili, Nino
Amatngalim, Gimano D
de Ligt, Joep
van Hoeck, Arne
Proost, Natalie
Begthel, Harry
Ramos, Emilio
Offerhaus, G Johan
Wiener, Dominique J
Dijkstra, Krijn K
Smit, Egbert F
Jonkers, Jos
Rios, Anne C
Voest, Emile E
Cuppen, Edwin
Coenjaerts, Frank E
Meyaard, Linde
Bont, Louis J
Peters, Peter J
Tans, Sander J
Boj, Sylvia F
Vries, Robert G
Beekman, Jeffrey M
Clevers, Hans
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 2019-01-14
Volume: 38
Issue: 4
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.15252/embj.2018100300
PMC: PMC6376275
OpenAlex: W2799736418
Cited by: 1,082
References: 82
Citations by year: 2026: 126 · 2025: 178 · 2024: 137 · 2023: 159 · 2022: 157 · 2021: 182 · 2020: 104 · 2019: 30
FWCI: 86.42
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0/ (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: The EMBO Journal (publishedVersion, cc-by-nc-nd)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion, cc-by-nc-nd)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
AMOLF Institutional Repository (AMOLF) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Research Publications (Maastricht University) (submittedVersion, cc-by-nc-nd)
Utrecht University Repository (Utrecht University) (submittedVersion, cc-by-nc-nd)
Funders: ZonMw (114021012, 40‐00812‐98‐14103, 91615182)
Human Frontier Science Program (CDA00076/2014‐C)
Prof. Dr. Jaap Swieringa Foundation (stAH‐CvM‐HI‐HC)
Dutch Cystic Fibrosis Society (HIT‐CF)
SU2C (SU2C‐AACR‐DT‐12‐14)
KWF Kankerbestrijding (2014‐7006)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (680‐47‐529, 834.11.002)
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
Keywords: airway organoids, cystic fibrosis, CFTR function, lung cancer, metastasis, respiratory syncytial virus, NS2 protein, neutrophil recruitment, disease modeling, Clara cells, ciliated cells
MeSH terms: Animals, Carcinoma, Non-Small-Cell Lung, Cells, Cultured, Cystic Fibrosis, Disease Models, Animal, Drug Screening Assays, Antitumor, Epithelial Cells, Female, Humans, Lung Neoplasms, Male, Organ Culture Techniques, Organoids, Respiratory Syncytial Viruses, Respiratory System, Mice, SCID, Mice, Inbred NOD, Respiratory Syncytial Virus Infections, Cystic Fibrosis Transmembrane Conductance Regulator, Xenograft Model Antitumor Assays, Mice

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