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Modelling human development and disease in pluripotent stem-cell-derived gastric organoids
Open accessAbstract
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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Generation of human colonic organoids from human pluripotent stem cells
Daoud, A., & Múnera, J. O. (2020) · Methods in cell biology · doi:10.1016/bs.mcb.2020.03.001 · Cited by 12
Pan, F. C., Evans, T., & Chen, S. (2020) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjaa031 · Cited by 12
Paediatric gastric organoids as a tool for disease modelling and clinical translation
Jones, B. C., Calà, G., Coppi, P. D., & Giobbe, G. G. (2021) · Pediatric Surgery International · doi:10.1007/s00383-020-04821-x · Cited by 12
Intestinal Enteroid Monolayers Model the Human Intestinal Environment for Escherichia coli Infection
Small, J. T., & Weiss, A. A. (2022) · Journal of Bacteriology · doi:10.1128/jb.00620-21 · Cited by 11
Däullary, T., Imdahl, F., Dietrich, O., Hepp, L., Krammer, T., Fey, C., Neuhaus, W., Metzger, M., Vogel, J., Westermann, A. J., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2186109 · Cited by 12
“In this context, we further measured an elevated median fluorescence intensity (MFI) of GFP, expressed by STm, at 16 h p.i. and 24 h p.i. in the OLFM4+ cells (Figure 3 e), indicating a link between the bacterial load of individual STm-infected cells and the upregulation of OLFM4.”
BackgroundMethodInfluentialRevolutionizing biomedical research: The imperative need for heart–kidney-connected organoids
Song, S.-S., Park, H., Kim, Y. K., & Kang, S. (2024) · APL Bioengineering · doi:10.1063/5.0190840 · Cited by 12
Marx, U., Accastelli, E., David, R. M., Erfurth, H., Koenig, L., Lauster, R., Ramme, A. P., Reinke, P., Volk, H., Winter, A., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.728866 · Cited by 15
Uehara, K., Koyanagi‐Aoi, M., Koide, T., Itoh, T., & Aoi, T. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.02.002 · Cited by 12
“Histological examinations by hematoxylin and eosin (H&E) staining at week 8 also revealed that the epithelium formed glandular or foveolar structures (Figure 1C), as in the previous report (McCracken et al., 2014).”
BackgroundMethodResultOrganoids: physiologically relevant ex vivo models for viral disease research
Wang, Y., Peng, D., Li, M., Meng, Y., Li, T., Li, S., Qiu, H., & Li, L. (2025) · Journal of Virology · doi:10.1128/jvi.01132-25 · Cited by 11
“The establishment of gastric organoids has advanced virus research (19).”
Organoids as Model Systems to Investigate Circadian Clock-Related Diseases and Treatments
Lee, S., & Hong, C. I. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.874288 · Cited by 13
The ATR inhibitor VE-821 increases the sensitivity of gastric cancer cells to cisplatin
Su, H., Yuan, Y., Tang, J., Zhang, Y., Wu, H., Zhang, Y., Liang, J., Wang, L., Zou, X., Huang, S., et al. (2023) · Translational Oncology · doi:10.1016/j.tranon.2023.101743 · Cited by 11
Yan, S., He, Y., Zhu, Y., Ye, W., Chen, Y., Zhu, C., Zhan, F., & Ma, Z. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1384450 · Cited by 12
Pluripotent stem cell‐derived organoids: A brief history of curiosity‐led discoveries
Lancaster, M. A. (2024) · BioEssays · doi:10.1002/bies.202400105 · Cited by 11
Retinoic Acid and the Development of the Endoderm
Kelly, G. M., & Drysdale, T. A. (2015) · Journal of Developmental Biology · doi:10.3390/jdb3020025 · Cited by 12
“This is surprising as RA is routinely used to generate endoderm from several undifferentiated embryonal carcinoma and embryonic stem cell lines [28–31].”
MethodStrategy to Establish Embryo-Derived Pluripotent Stem Cells in Cattle
Kim, D., & Roh, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22095011 · Cited by 11
Rego, S. L., Zakhem, E., Orlando, G., & Bitar, K. N. (2015) · Methods · doi:10.1016/j.ymeth.2015.08.014 · Cited by 11
Modeling Human Nutrition Using Human Embryonic Stem Cells
Ben‐Zvi, D., & Melton, D. A. (2015) · Cell · doi:10.1016/j.cell.2015.02.039 · Cited by 11
Investigating pediatric disorders with induced pluripotent stem cells
Durbin, M. D., Cadar, A. G., Chun, Y. W., & Hong, C. C. (2018) · Pediatric Research · doi:10.1038/s41390-018-0064-2 · Cited by 11
“A 3D gastric organoid was created that progresses through developmental stages adopts similar architecture to the stomach.(54) This organoid provided valuable insights into the gut development, as well as H.”
BackgroundMethodDaoud, A., & Múnera, J. O. (2019) · Frontiers in Medicine · doi:10.3389/fmed.2019.00297 · Cited by 11
“This system has been instrumental to studying the expression of regionally expressed enteroendocrine hormones (7, 34, 35).”
BackgroundTogo, S., Sato, K., Kawamura, R., Kobayashi, N., Noiri, M., Nakabayashi, S., Teramura, Y., & Yoshikawa, H. (2020) · APL Bioengineering · doi:10.1063/1.5123749 · Cited by 11
“Tissues in a Dish”: A Review of Organoids in Plastic Surgery
Chinta, M. S., desJardins-Park, H. E., Wan, D. C., & Longaker, M. T. (2020) · Plastic & Reconstructive Surgery Global Open · doi:10.1097/gox.0000000000002787 · Cited by 11
Modeling Gastrointestinal Diseases Using Organoids to Understand Healing and Regenerative Processes
Ollivier, A., Mahé, M. M., & Guasch, G. (2021) · Cells · doi:10.3390/cells10061331 · Cited by 11
“Gastric organoids had been first established from LGR5+ stomach adult stem cells [45], and later on from pluripotent stem cells [46].”
BackgroundLui, K. N.-C., & Ngan, E. (2022) · Cells · doi:10.3390/cells11213428 · Cited by 12
“By resembling the embryonic intestinal development with a series of growth factor manipulations, hPSCs can be induced into the endodermal lineage to generate intestinal epithelium, which can later self-organize into a 3-D organ-like structure called intestinal organoids (HIOs) [20,21].”
BackgroundCan an Organoid Recapitulate the Metabolome of its Parent Tissue? A Pilot NMR Spectroscopy Study
Bhattacharya, P. K. (2017) · Journal of Cancer Prevention & Current Research · doi:10.15406/jcpcr.2017.08.00307 · Cited by 11
“These unique morphological and cellular properties make organoids an excellent model to study development, infectious disease, and signaling pathways [5].”
BackgroundCapturing Stem Cell Behavior Using Intravital and Live Cell MicroscopyPreprint
Fumagalli, A., Bruens, L., Scheele, C. L. G. J., & van Rheenen, J. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a035949 · Cited by 12
Zhao, H., Collet, C., Peng, D., Sinha, U. K., & Lin, D. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.09.026 · Cited by 9
Animal Models of Helicobacter pylori Infection and Vaccines: Current Status and Future Prospects
Liu, Z., Li, H., Huang, X., & Liu, Q. (2024) · Helicobacter · doi:10.1111/hel.13119 · Cited by 10
SMPD4 -mediated sphingolipid metabolism regulates brain and primary cilia development
Inskeep, K. A., Crase, B., Dayarathna, T. K., & Stottmann, R. W. (2024) · Development · doi:10.1242/dev.202645 · Cited by 9
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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