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Modelling human development and disease in pluripotent stem-cell-derived gastric organoids
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Gastric diseases, including peptic ulcer disease and gastric cancer, affect 10% of the world's population and are largely due to chronic Helicobacter pylori infection. Species differences in embryonic development and architecture of the adult stomach make animal models suboptimal for studying human stomach organogenesis and pathogenesis, and there is no experimental model of normal human gastric mucosa. Here we report the de novo generation of three-dimensional human gastric tissue in vitro through the directed differentiation of human pluripotent stem cells. We show that temporal manipulation of the FGF, WNT, BMP, retinoic acid and EGF signalling pathways and three-dimensional growth are sufficient to generate human gastric organoids (hGOs). Developing hGOs progressed through molecular and morphogenetic stages that were nearly identical to the developing antrum of the mouse stomach. Organoids formed primitive gastric gland- and pit-like domains, proliferative zones containing LGR5-expressing cells, surface and antral mucous cells, and a diversity of gastric endocrine cells. We used hGO cultures to identify novel signalling mechanisms that regulate early endoderm patterning and gastric endocrine cell differentiation upstream of the transcription factor NEUROG3. Using hGOs to model pathogenesis of human disease, we found that H. pylori infection resulted in rapid association of the virulence factor CagA with the c-Met receptor, activation of signalling and induction of epithelial proliferation. Together, these studies describe a new and robust in vitro system for elucidating the mechanisms underlying human stomach development and disease.
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“Thus, RA is crucial for human posterior foregut specification, consistent with the role for RA in generating foregut derivatives such as stomach endoderm in vitro (McCracken et al., 2014) and how inhibiting RA synthesis abrogates both liver and pancreas formation in zebrafish embryos (Stafford and Prince, 2002).”
From A Roadmap for Human Liver Differentiation from Pluripotent Stem Cells (2018) · cites this paper as McCracken et al., 2014
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Biomedical applications of organoids derived from the digestive system
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Skin Organoid Research Progress and Potential Applications
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Establishment and characterization of adult human gastric epithelial progenitor‐like cell lines
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“first induced embryonic stem cells (ESCs) into gastric antrum epithelial structure.(41) These two studies laid the foundation for different culture methods of human gastric organoids.”
BackgroundGastric stem cell research and gastric organoids
Jeong, H., & Nam, K. T. (2022) · Organoid · doi:10.51335/organoid.2022.2.e27 · Cited by 2
“acute host response, including c-Met phosphorylation and proliferation [65].”
BackgroundMethodHuman Organoids, their Perspective, and Applications for Personalized Therapy: Rapid Review
Pratap, P. D., & Ahmad, S. (2023) · Global Journal of Medical Pharmaceutical and Biomedical Update · doi:10.25259/gjmpbu_96_2022 · Cited by 2
Rossi, S. A., García-Barbazán, I., Chamorro-Herrero, I., Taborda, C. P., Zaragoza, Ó., & Zambrano, A. (2023) · Microbes and Infection · doi:10.1016/j.micinf.2023.105260 · Cited by 2
Profiling Luminal pH in Three-Dimensional Gastrointestinal Organoids Using Microelectrodes
Lyon, K. N., Bansil, R., & Bimczok, D. (2024) · Journal of Visualized Experiments · doi:10.3791/66900 · Cited by 2
Qin, Z., Fang, Y., Liu, Y., Zhang, L., Zhang, R., & Zhang, S. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1509269 · Cited by 2
Organoids and derived models to study the microenvironments of bacterial infections
Lyon, K. N., Eng, K. Y., Boccellato, F., & D’Amore, A. (2025) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2025.100595 · Cited by 2
Du, L., Cheng, Z., Si, Z., Zhou, Z., Ma, Y., Zhang, B., Zhao, Y., Gong, T., Yang, M., Xu, H., et al. (2025) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2025.108780 · Cited by 2
The use of stem cells and organoids for modeling host-microbe interactions in low-biomass tissues
Shaw, C. A., Verstraete, M., Graniczkowska, K. B., Risoen, K. R., Dini, P., & Weimer, B. C. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1641366 · Cited by 2
Sweet Relief: Reprogramming Gastric Endocrine Cells to Make Insulin
McCauley, H. A., & Wells, J. M. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.02.009 · Cited by 2
“To move this technology forward, researchers will need to determine if human gastric tissues, derived from patient biopsies (Bartfeld et al., 2015) or from human pluripotent stem cells (McCracken et al., 2014), are competent to generate functional insulin-expressing cells.”
BackgroundSelf-citationAt new heights – endodermal lineages in development and disease
Ober, E. A., & Grapin‐Botton, A. (2015) · Development · doi:10.1242/dev.121095 · Cited by 2
“James Wells’ lab showed how increased FGF and WNT levels, together with inhibition of the BMP pathway and RA activation, promote posterior foregut formation and, eventually, organoids resembling antral stomach (McCracken et al., 2014); fundal fate was obtained bymore sustainedWNT and FGF signaling.”
Sáenz, J. B., & Mills, J. C. (2017) · Nature · doi:10.1038/nature21110 · Cited by 2
Varga, A., Kumar, J. D., Simpson, A. W. M., Dodd, S., Hegyi, P. J., Dockray, G. J., & Varró, A. (2017) · Physiological Reports · doi:10.14814/phy2.13394 · Cited by 2
“These cells may originate by epithelial-mesenchymal transition (McCracken et al. 2014), from inward migration of bone-marrow derived mesenchymal stem cells (Quante et al.”
BackgroundAlternative methods to animal experimentation for testing developmental toxicity
Pamies, D., Estevan, C., Vilanova, E., & Sogorb, M. A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-89773-0.00007-2 · Cited by 2
Analysing Genetic Programs of Cell Differentiation to Study Cardiac Cell Diversification
Wu, Z., Shen, S., Sun, Y., Werner, T., Bradford, S. T., & Palpant, N. J. (2022) · Springer eBooks · doi:10.1007/978-3-030-86140-7_8 · Cited by 1
The Cell Biology of Gastric Acid Secretion
Okamoto, C. T., Asano, S., & 酒井, 秀. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809954-4.00038-4 · Cited by 3
Soleas, J. P., Huang, L., D’Arcangelo, E., Nostro, M. C., Waddell, T. K., McGuigan, A. P., & Karoubi, G. (2021) · Bioengineering · doi:10.3390/bioengineering8120209 · Cited by 2
Rajamani, U., Gross, A. R., Ocampo, C., Andres, A. M., Gottlieb, R. A., & Sareen, D. (2019) · Nature Communications · doi:10.1038/s41467-019-08572-9 · Cited by 2
RetractedMicrofluidics in Microbiome and Cancer Research
Udayasuryan, B., Slade, D. J., & Verbridge, S. S. (2019) · doi:10.1002/9783527818341.ch9 · Cited by 2
In-Vitro 3-Dimensional Organoid Models – A Concise Review on Clinical Importance
Bairagi, R., & Patil, R. (2024) · International Journal of Pharmaceutical Sciences and Nanotechnology · doi:10.37285/ijpsn.2024.17.1.8 · Cited by 1
The establishment of organoids and their applications
Han, W.-J. (2025) · New discovery. · doi:10.61958/ndnu9408 · Cited by 1
Zhang, X., Sun, S., Cheng, S., Dai, J., Du, F., Wang, J., Wei, D., Yan, Y., & Liu, Y. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1601688 · Cited by 1
The way forward: Towards pragmatic preclinical microbiome research in inflammatory bowel disease
Petito, V., Deleu, S., Lopetuso, L. R., Pizarro, T. T., & Scaldaferri, F. (2025) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2025.102054 · Cited by 1
An overview on organoids—Past, present, and future scenarios of organoids
Iyer, M. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-29898-1.00007-1 · Cited by 1
Advances in sweat gland organoids: construction, molecular mechanisms, and challenges
Liu, X., Ye, Y., Chen, J., Tan, Y., Yang, G., Li, L., Liu, H. S., Liang, Y., Lei, M., & Lei, X. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04689-5 · Cited by 1
“These miniature, functional tissue models have emerged as powerful tools for drug screening, disease modeling, and tissue repair/regeneration, providing unprecedented insights into cellular behavior and therapeutic development [7–14].”
The Future Pioneered by Intestinal Organoid Culture Technology
Okamoto, K., Shinomiya, R., Ueda, H., Kawaguchi, T., Kagemoto, K., Okada, Y., Kawano, Y., Sogabe, M., Miyamoto, H., Sato, Y., et al. (2025) · The Journal of Medical Investigation · doi:10.2152/jmi.72.235 · Cited by 1
Research insights and clinical opportunities of functional organoid-based platforms
Huang, Y., Shen, W., Li, K., Zhang, Y., Lv, Q., Wang, C., Mao, W., & Zhao, A. (2025) · Bio-Design and Manufacturing · doi:10.1631/bdm.2400519 · Cited by 1
Kechele, D. O., Enriquez, J. R., Eicher, A. K., Thorner, K., Chaturvedi, P., Kishimoto, K., Adair, B., Sanchez, J. G., Tominaga, K., Zorn, A. M., et al. (2026) · Development · doi:10.1242/dev.205196 · Cited by 1
Self-citationGastric cancer organoids and their convergence in engineering approaches
Lim, S., Kim, S. H., Hye‐Jin, J., Park, S., Koo, B., Lee, J., & Shin, W. (2026) · FEBS Letters · doi:10.1002/1873-3468.70272 · Cited by 2
Chen, Y., Xu, N. L. J., Dong, M., Liu, W., Liu, Z., Sun, G., & Jia, Y. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1773734 · Cited by 2
Metadata
- Authors
- McCracken, K. W., Catá, E. M., Crawford, C. M., Sinagoga, K. L., Schumacher, M., Rockich, B. E., Tsai, Y.-H., Mayhew, C. N., Spence, J. R., Zavros, Y., & Wells, J. M.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- University of Cincinnati (US)
- University of Michigan (US)
- Corresponding author
- Zavros, Yana
- Wells, James M.
- ORCID
- Venue
- Nature
- Published
- 2014-10-29
- Volume
- 516
- Issue
- 7531
- Pages
- 400-404
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4270898
- OpenAlex
- W2054186703
- Cited by
- 980
- References
- 43
- Citations by year
- 2026: 54 · 2025: 67 · 2024: 87 · 2023: 69 · 2022: 104 · 2021: 106 · 2020: 96 · 2019: 79 · 2018: 82 · 2017: 93 · 2016: 86 · 2015: 50 · 2014: 6
- FWCI
- 32.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (5ul1rr026314-03)
- National Institute of General Medical Sciences (T32GM063483, R01GM072915)
- National Institute of Allergy and Infectious Diseases (U19AI116491)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK034933, K01DK091415, P30 DK0789392, R01DK083402, R01DK098350, R01DK080823, R01DK092456, P30DK078392)
- National Center for Research Resources (UL1-RR026314, U54-RR-025216)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Gastroenterology › Helicobacter pylori-related gastroenterology studies
- Keywords
- gastric organoids, human pluripotent stem cells, induced pluripotent stem cells, human embryonic stem cells, gastric epithelium, Helicobacter pylori infection, CagA, c-Met, gastric endocrine cells, Lgr5, Neurog3, signaling pathways, peptic ulcer, gastric cancer, in vitro disease model
- MeSH terms
- Cell Differentiation, Humans, Models, Biological, Organoids, Stomach, Signal Transduction, Helicobacter pylori, Helicobacter Infections, Organogenesis, Pluripotent Stem Cells
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