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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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“Although recapitulating mammalian organ structure in vitro is challenging, many protocols have been reported over the past 15 years, including organoids of the intestine [3], stomach [4], retina [5], cerebra [6], liver [7,8], kidney [9], prostate [10], lung [11], and others.”
BackgroundOrganoid modeling meets cancers of female reproductive tract
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“In addition to a few organoids that only need endogenous signals for formation [25], most organoids require exogenous growth factors throughout [26, 27] or at least in the initial phase [28] of the culture process to help cells to self-organize and gradually divide and differentiate along…”
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Idowu, S., Bertrand, P. P., & Walduck, A. K. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052790 · Cited by 9
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He, Z., Hu, X.-H., He, T.-Y., & Zhao, T. (2024) · iScience · doi:10.1016/j.isci.2024.109465 · Cited by 8
“78 79–81 Furthermore, a SMA+ myofibroblast (MF) niche cells express Wnt5a, BMP4, and IL-6, among other factors, which sustain the stem cell niche and facilitate early tumor self-renewal.”
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“Similarly, intestinal, lung, gastric, and brain organoids have been applied to model infectious diseases, including Cryptosporidium (153), Middle East respiratory syndrome coronavirus (154), Helicobacter pylori (155, 156), influenza virus”
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“Finally, and perhaps most interestingly, temporal activation of WNT/β-catenin signaling promoted the development of corpuslike organoids at the expense of antral organoids (McCracken et al., 2014; Broda et al., 2019).”
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“Both of these lines have been previously characterized [34,35].”
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“Therefore, to validate that the G4KD-hiPSC line generated in our laboratory was similarly capable of generating DE, we examined two transcription factors essential for DE differentiation, FOXA2 and SOX17 (6, 7, 26), at day 3.”
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“1b) results in a stronger immune response by gland cells than pit cells, in particular regarding the pro-inflammatory nuclear factor-κ light chain-enhancer of activated B cells (NF-κB) response 37–40 .”
State of the Art in 3D Culture Models Applied to Thyroid Cancer
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“238,239 In addition, microvascular network remodeling includes angiogenesis, determined as the germinating of new capillaries and network modeling related to the formation and linkage of available vessels.”
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BackgroundThe Histopathological Types and Distribution Characteristics of Gastric Mixed Tumors
Zhu, F.-H., Wang, Y., Zhou, J., Meng, N.-L., Wang, Y., Jiang, B., & Wang, S. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.873005 · Cited by 7
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“These structures overcome the limitations of traditional 2D neural cultures such as the lack of supporting cell types and spatial structure, offering a closer approximation of the complexity of the human brain [12,13].”
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“Furthermore, NGO can mimic the glandular structure and biological functions observed in vivo (47), making it an optimal choice for in vitro disease modeling in studying GC pathogenesis.”
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Organoid Modeling and Single-Cell Profiling Reveal Smooth Muscle Cell Migration in Moyamoya Disease
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Mastering Organoid Growth: A Complete Guide to Overcoming Methodological Challenges
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“In contrast, intestinal organoids, require Wnt [ 126–128 ], and FGF signaling for “posteriorization” to a develop polarized intestinal epithelium with villus like structures and crypt like zones [ 59, 65 ].”
Human stem cell-based embryo models: innovation, ethics, and policy
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“This has been done with some success in the case of PSC-derived neuronal (Velasco et al ., 2020; Sidhaye and Knoblich, 2021) and intestinal (McCracken et al ., 2014; Aurora and Spence, 2016) organoids.”
Generation of human gastric assembloids from primary fetal organoids
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“Indeed, while many of the studies concerning stomach development have been carried out in rodents [4–8], this knowledge has led to the successful generation of human gastric organoids through direct differentiation from induced pluripotent stem cells [9, 10].”
Advances in the study of gastric organoids as disease models
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The Formation of Human Arteriovenous Malformation Organoids and Their Characteristics
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Geometrically engineered organoid units and their assembly for pre-construction of organ structures
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Met Activation and Carcinogenesis
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Revisiting the immunocytochemical detection of Neurogenin 3 expression in mouse and man
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Studying the Role of Chromosomal Instability (CIN) in GI Cancers Using Patient-derived Organoids
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Organoids as tools for fundamental discovery and translation—a Keystone Symposia report
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“For example, because they are grown as 3-dimensional structures in a droplet of extracellular matrix, their culture can be cumbersome, and accessing the apical (luminal) surface of the epithelium is difficult and requires time-consuming and labor-intensive approaches, such as microinjection.(3,4) Three-dimensional cul…”
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“…organoid [16], liver organoid [17], cerebral organoid [18], salivary organoid [19], prostate organoid [20], lung organoid [21], gastric organoid [22], mammary gland organoid [23], kidney organoid [24], placenta organoid [25], skin organoid [26], etc. Organoids were recognized for their…”
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“To date, numerous research groups have succeeded in obtaining iPSC-derived organoids consisting of epithelial cells, such as lung organoids,[15–17] organoids of the sensory epithelium of the inner ear,[18] gastric organoids,[19] liver,[20] intestines,[21] and thyroid gland.”
BackgroundOrganoides: fundamentos, presente y futuro
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“intestines, and many more, allowing the modeling of both normal and sick organs (1-5); and have the potential to reproduce biological developmental processes (6,7).”
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An Exploration of Organoid Technology: Present Advancements, Applications, and Obstacles
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“147 Furthermore, the induction of epithelial proliferation was investigated by infecting human and murine gastric organoids with H. pylori and examining the role of CD44.”
BackgroundThe application of organoids in cancers associated with pathogenic infections
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“For instance, McCracken et al. [18] successfully generated human gastric organoids (hGOs) in vitro through the directed differentiation of human pluripotent stem cells.”
BackgroundMethodInfluentialIntestinal stem cell niche: An upcoming area of immense importance in gastrointestinal disorders
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“Pluripotent stem cell-derived gastric organoids have successfully demonstrated the association of CagA + Helicobacter pylori -induced peptic ulcer disease with gastric carcinoma [122].”
Construction methods and latest applications of kidney cancer organoids
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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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