ArticleCell stem cell2018
3D Modeling of Esophageal Development using Human PSC-Derived Basal Progenitors Reveals a Critical Role for Notch Signaling.
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Article in Cell stem cell, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 64 papers.
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64citing papers in PubMed
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Who cites it
64 citing papers in PubMed, 98 citations in OpenAlex.
- Closing the gap: Toward functional, bioengineered esophageal grafts.Cell stem cell · 2026Article
- Intrinsic mechanisms and microenvironmental cues fine-tune plasticity of esophageal progenitors.Nature communications · 2026Article
- Review
- VSIG10L is a major determinant of esophageal homeostasis and inherited predisposition to Barrett's esophagus.Nature communications · 2026Article
- Targeting notch signaling pathway in esophageal cancer: from molecular insights to therapies.Oncology reviews · 2026Review
- Genetic Engineering of Esophageal Organoids: CRISPR-Based Knock-In for Cell Lineage Tracing.Methods in molecular biology (Clifton, N.J.) · 2025Article
- A spatiotemporal and machine-learning platform facilitates the manufacturing of hPSC-derived esophageal mucosa.Developmental cell · 2025Article
- The next frontier in lung development and regeneration research: harnessing iPSC models to illuminate notch signaling pathways.Frontiers in cell and developmental biology · 2025Review
- Epithelial architecture and signaling activity in the adult human esophagus.Frontiers in cell and developmental biology · 2025Review
- Identifying the Role of YAP in the Development of Rumen Epithelium Using 3D Organoid.Stem cells international · 2025Article
- Biomedical applications of organoids derived from the digestive system.Frontiers in cell and developmental biology · 2025Review
- Epigenetic regulation of p63 blocks squamous-to-neuroendocrine transdifferentiation in esophageal development and malignancy.Science advances · 2024Article
- Self-sustaining long-term 3D epithelioid cultures reveal drivers of clonal expansion in esophageal epithelium.Nature genetics · 2024Article
- Directed differentiation of human embryonic stem cells into parathyroid cells and establishment of parathyroid organoids.Cell proliferation · 2024Article
- The role of the fibroblast in Barrett's esophagus and esophageal adenocarcinoma.Current opinion in gastroenterology · 2024Review
- Jag1/2 maintain esophageal homeostasis and suppress foregut tumorigenesis by restricting the basal progenitor cell pool.Nature communications · 2024Article
- Reciprocal Interactions Between the Epithelium and Mesenchyme in Organogenesis.Results and problems in cell differentiation · 2024Article
- Establishing mouse and human oral esophageal organoids to investigate the tumor immune response.Disease models & mechanisms · 2024Article
- Modelling esophageal adenocarcinoma and Barrett's esophagus with patient-derived organoids.Frontiers in molecular biosciences · 2024Review
- Targeting the SOX2/CDP protein complex with a peptide suppresses the malignant progression of esophageal squamous cell carcinoma.Cell death discovery · 2023Article
4 more citing papers are in PubMed but not listed here.
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Authors and funding
21 authors at 7 institutions in 4 countries.
Yongchun ZhangDivision of Digestive and Liver Diseases, Department of Medicine, Columbia University, New York, NY 10032, USA; Columbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA.
Ying YangColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Department of Genetics and Development, Columbia University Medical Center, New York, NY 10032, USA.
Ming JiangDivision of Digestive and Liver Diseases, Department of Medicine, Columbia University, New York, NY 10032, USA; Columbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA.
Sarah Xuelian HuangColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Columbia Center for Translational Immunology, Columbia University Medical Center, New York, NY 10032, USA.
Wanwei ZhangDepartment of Microbiology and Immunology, Columbia University Medical Center, New York, NY 10032, USA.
Denise Al AlamDevelopmental Biology and Regenerative Medicine Program, Department of Pediatric Surgery, The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA, USA; Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Soula DanopoulosDevelopmental Biology and Regenerative Medicine Program, Department of Pediatric Surgery, The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA, USA; Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Munemasa MoriColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA.
Ya-Wen ChenColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Columbia Center for Translational Immunology, Columbia University Medical Center, New York, NY 10032, USA.
Revathi BalasubramanianDepartment of Ophthalmology, Columbia University, New York, NY 10032, USA; Department of Pathology and Cell Biology, Columbia University, New York, NY 10032, USA.
Susana M Chuva de Sousa LopesDepartment of Anatomy and Embryology, Leiden University Medical Center, Leiden, Netherlands; Department for Reproductive Medicine, Ghent University Hospital, Ghent, Belgium.
Carlos SerraColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA.
Monika BialeckaDepartment of Anatomy and Embryology, Leiden University Medical Center, Leiden, Netherlands.
Eugene KimDivision of Digestive and Liver Diseases, Department of Medicine, Columbia University, New York, NY 10032, USA.
Sijie LinDivision of Digestive and Liver Diseases, Department of Medicine, Columbia University, New York, NY 10032, USA.
Ana Luisa Rodrigues Toste de CarvalhoColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Columbia Center for Translational Immunology, Columbia University Medical Center, New York, NY 10032, USA; Department of Microbiology and Immunology, Columbia University Medical Center, New York, NY 10032, USA; Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, 4710-057 Braga, Portugal; ICVS/3B's, PT Government Associate Laboratory, 4710-057 Braga/Guimarães, Portugal.
Paul N RiccioColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA.
Wellington V CardosoColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Department of Genetics and Development, Columbia University Medical Center, New York, NY 10032, USA.
Xin ZhangDepartment of Ophthalmology, Columbia University, New York, NY 10032, USA; Department of Pathology and Cell Biology, Columbia University, New York, NY 10032, USA.
Hans-Willem SnoeckColumbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA; Columbia Center for Translational Immunology, Columbia University Medical Center, New York, NY 10032, USA; Department of Microbiology and Immunology, Columbia University Medical Center, New York, NY 10032, USA.
Jianwen QueDivision of Digestive and Liver Diseases, Department of Medicine, Columbia University, New York, NY 10032, USA; Columbia Center for Human Development, Columbia University Medical Center, New York, NY 10032, USA. Electronic address: jq2240@cumc.columbia.edu.
Columbia University Irving Medical Center · USColumbia University · USChildren's Hospital of Los Angeles · USGhent University Hospital · BELeiden University Medical Center · NLUniversity of Minho · PTUniversity of Southern California · US
Funding
Signaling Mechanisms of Lens DevelopmentR01EY017061 · NEI · INDIANA UNIV-PURDUE UNIV AT INDIANAPOLIS · PI ZHANG, XIN · 2006 to 2025
$9.0MModeling, pathogenesis and treatment of idiopathic pulmonary fibrosisU01HL134760 · NHLBI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI SNOECK, HANS-WILLEM E, VUNJAK-NOVAKOVIC, GORDANA · 2016 to 2022
$8.5MMechanisms Controlling Expansion and Lineage Specification of Airway Progenitors in Development and DiseaseR35HL135834 · NHLBI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI CARDOSO, WELLINGTON V. · 2017 to 2023
$6.7MRegulation of FGF signaling in lacrimal gland developmentR01EY018868 · NEI · INDIANA UNIVERSITY INDIANAPOLIS · PI Xin Zhang · 2009 to 2026
$6.3MBasal Progenitor Cells and Eosinophilic EsophagitisR01DK100342 · NIDDK · UNIVERSITY OF ROCHESTER · PI QUE, JIANWEN · 2014 to 2022
$3.3MPDGF signaling in lens developmentR01EY025933 · NEI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI ZHANG, XIN · 2015 to 2023
$3.2MNkx2.1+ Lung-Derived Cells in Asthma and Eosinophilic Esophagitis (EoE)R01HL132996 · NHLBI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI QUE, JIANWEN · 2017 to 2020
$2.0MBarrett's esophagus and progenitor cells at the squamous-columnar junctionR01DK113144 · NIDDK · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI QUE, JIANWEN · 2017 to 2020
$1.4MBD Biosciences InfluxS10OD020056 · OD · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI SNOECK, HANS-WILLEM E · 2015 to 2015
$600kNEI NIH HHS R01 EY017061NEI NIH HHS R01 EY018868NEI NIH HHS R01 EY025933NHLBI NIH HHS R01 HL132996NHLBI NIH HHS R35 HL135834NHLBI NIH HHS U01 HL134760NIDDK NIH HHS R01 DK100342NIDDK NIH HHS R01 DK113144NIH HHS S10 OD020056
Abstract
Pluripotent stem cells (PSCs) could provide a powerful system to model development of the human esophagus, whose distinct tissue organization compared to rodent esophagus suggests that developmental mechanisms may not be conserved between species. We therefore established an efficient protocol for generating esophageal progenitor cells (EPCs) from human PSCs. We found that inhibition of TGF-ß and BMP signaling is required for sequential specification of EPCs, which can be further purified using cell-surface markers. These EPCs resemble their human fetal counterparts and can recapitulate normal development of esophageal stratified squamous epithelium during in vitro 3D cultures and in vivo. Importantly, combining hPSC differentiation strategies with mouse genetics elucidated a critical role for Notch signaling in the formation of this epithelium. These studies therefore not only provide an efficient approach to generate EPCs, but also offer a model system to study the regulatory mechanisms underlying development of the human esophagus.
Indexed as
Imaging, Three-DimensionalSignal TransductionAnimalsEsophagusHumansMiceMice, Inbred C57BLMice, Inbred NODPluripotent Stem CellsReceptors, NotchReceptors, Notchbasal cellsBMPesophagushuman embryonic stem cellshuman-induced pluripotent stem cellNOTCHorganoidsTGF-ßWNT
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