ArticleGastroenterology2023
SOX9 Modulates the Transformation of Gastric Stem Cells Through Biased Symmetric Cell Division.
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Article in Gastroenterology, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 41 papers, 1 of them a synthesis that pooled it.
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41citing papers in PubMed, 1 pooled it
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41 citing papers in PubMed, 1 synthesis or guideline pooled it, 50 citations in OpenAlex.
- Dynamic role of gastric stem cells and chief cells in precancerous lesions of gastric cancer: global knowledge mapping and emerging trends based on bibliometric analysis from 2004 to 2024.Frontiers in oncology · 2025Pooled it
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- Wnt regulates cellular differentiation and retinoid metabolism genes in the mouse stomach.American journal of physiology. Gastrointestinal and liver physiology · 2026Article
- The STAT3-CCND2 Axis Drives a Proliferative Metaplastic Precursor Population in Gastric Intestinal Metaplasia.Journal of cellular and molecular medicine · 2026Article
- Targeting APE1-Redox Function Reverses SOX9-mediated Chemoresistance in Esophageal Adenocarcinoma.Gastroenterology · 2026Article
- Single-nucleus multiome sequencing identifies candidate regulators of mouse gastric epithelial homeostasis.bioRxiv : the preprint server for biology · 2026Article
- Aneuploidy in exfoliated buccal cells: mechanisms, methods, and future perspectives.Mutagenesis · 2026Review
- Oncogenic SOX9-TRAIP signaling drives gastric cancer progression by mediating the degradation of the CPEB3-mTORC1 tumor suppressor axis.World journal of surgical oncology · 2026Article
- Recent advances in spasmolytic polypeptide expressing metaplasia research.World journal of gastrointestinal oncology · 2026Review
- Weimishu prescription alleviates liver-stomach disharmony and chronic gastritis by reducing inflammation and regulating gastric stem cell differentiation.Journal of traditional Chinese medicine = Chung i tsa chih ying wen pan · 2026Article
- Identification of LGR5 and TFF2 as Biomarkers in High-Risk Chronic Atrophic Gastritis: From Multi-Omics Mining to Clinical Validation.Digestion · 2026Article
- Gastrin-dependent expansion of Cck2rGut · 2026Article
- Regulation and Function of Sox2 and CD44 Expression in the Stomach by Bone Morphogenetic Protein Signaling.Gastro hep advances · 2026Article
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- The SOX4-Semaphorin3C axis promotes esophageal adenocarcinoma progression.Cancer letters · 2025Article
- CDK1 drives SOX9-mediated chemotherapeutic resistance in gastric cancer.Journal of experimental & clinical cancer research : CR · 2025Article
- Increased Fos immunoreactivity in astrocytes in the raphe pallidus under hypoxia, not hypercapnia.Histochemistry and cell biology · 2025Article
- SOX-9 as a prognostic marker in gastric adenocarcinoma.Biomolecules & biomedicine · 2025Article
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Authors and funding
22 authors at 5 institutions in 2 countries.
Qiyue ChenDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Columbia Center for Human Development, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Division of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Kai WengDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Mi LinDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Columbia Center for Human Development, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Division of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Ming JiangNational Clinical Research Center for Child Health of the Children's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of China.
Yinshan FangColumbia Center for Human Development, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Sanny S W ChungColumbia Center for Human Development, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Xiaobo HuangDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Qing ZhongDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Zhiyu LiuDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Zening HuangDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Jianxian LinDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Ping LiDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China.
Wael El-RifaiDepartment of Surgery, University of Miami, Miami, Florida; Department of Veterans Affairs, Miami Healthcare System, Miami, Florida.
Alexander ZaikaDepartment of Surgery, University of Miami, Miami, Florida; Department of Veterans Affairs, Miami Healthcare System, Miami, Florida.
Haiyan LiDepartment of Pathology & Laboratory Medicine, Roswell Park Comprehensive Cancer Center, Buffalo, New York.
Anil K RustgiDivision of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Hiroshi NakagawaDivision of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Julian A AbramsDivision of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Timothy C WangDivision of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York.
Chao LuDepartment of Genetics and Development, Columbia University Irving Medical Center, New York, New York.
Changming HuangDepartment of Gastric Surgery, Fujian Medical University Union Hospital, Fuzhou, Fujian, People's Republic of China; Key Laboratory of Ministry of Education of Gastrointestinal Cancer, Fujian Medical University, Fuzhou, Fujian, People's Republic of China; Fujian Key Laboratory of Tumor Microbiology, Fujian Medical University, Fuzhou, Fujian, People's Republic of China. Electronic address: hcmlr2002@163.com.
Jianwen QueColumbia Center for Human Development, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Division of Digestive and Liver Diseases, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York; Herbert Irving Comprehensive Cancer Center, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, New York, New York. Electronic address: jq2240@cumc.columbia.edu.
Fujian Medical University · CNColumbia University Irving Medical Center · USUniversity of Miami · USChildren's Hospital of Zhejiang University · CNRoswell Park Comprehensive Cancer Center · US
Funding
Tumor Biology and Microenvironment ProgramP30CA013696 · NCI · COLUMBIA UNIV NEW YORK MORNINGSIDE · PI Anil K Rustgi · 1985 to 2026
$115.3MTransformed Esophageal Epithelial Cells and the Tumor MicroenvironmentP01CA098101 · NCI · UNIVERSITY OF PENNSYLVANIA · PI RUSTGI, ANIL K · 2003 to 2023
$31.7MSOX4-Mediated Transcription Program in Esophageal AdenocarcinomaP01CA268991 · NCI · UNIVERSITY OF MIAMI SCHOOL OF MEDICINE · PI WAEL EL-RIFAI · 2022 to 2026
$9.2MThe Organoid and Cell Culture CoreP30DK132710 · NIDDK · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI Robert F. Schwabe · 2022 to 2026
$7.2MGastroesophageal junction stem cells as the origin of Barretts esophagus and cancerR01CA272901 · NCI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI QUE, JIANWEN, WANG, TIMOTHY CRAGIN · 2022 to 2025
$4.9MRegulation of the Oncogenic Stress Response in Helicobacter pylori-infected cellsR01CA138833 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI ALEXANDER I. ZAIKA · 2010 to 2026
$4.3MBasal Progenitor Cells and Eosinophilic EsophagitisR01DK100342 · NIDDK · UNIVERSITY OF ROCHESTER · PI QUE, JIANWEN · 2014 to 2022
$3.3MAutophagy and esophageal tissue remodeling in EoER01DK114436 · NIDDK · UNIVERSITY OF PENNSYLVANIA · PI NAKAGAWA, HIROSHI · 2017 to 2024
$3.1MCell Fate Regulation in Esophageal Progenitor CellsR01DK132251 · NIDDK · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI LU, CHAO, QUE, JIANWEN · 2022 to 2025
$2.3MMolecular Functions of CDK1 in Gastric TumorigenesisR01CA249949 · NCI · UNIVERSITY OF MIAMI SCHOOL OF MEDICINE · PI EL-RIFAI, WAEL · 2021 to 2025
$2.3MIntercepting novel functions of AURKA in gastric tumorigenesisR01CA266528 · NCI · UNIVERSITY OF MIAMI SCHOOL OF MEDICINE · PI EL-RIFAI, WAEL · 2022 to 2025
$2.2MSignaling Mechanisms Promoting Barrett’s MetaplasiaR01DK120650 · NIDDK · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI QUE, JIANWEN · 2019 to 2022
$1.8MBLRD VA I01 BX001179BLRD VA I01 BX002115BLRD VA IK6 BX003787BLRD VA IK6 BX006300NCI NIH HHS P01 CA098101NCI NIH HHS P01 CA268991NCI NIH HHS P30 CA013696NCI NIH HHS R01 CA138833NCI NIH HHS R01 CA249949NCI NIH HHS R01 CA266528NCI NIH HHS R01 CA272901NCRR NIH HHS S10 RR027050NIDDK NIH HHS P30 DK132710NIDDK NIH HHS R01 DK100342NIDDK NIH HHS R01 DK113144NIDDK NIH HHS R01 DK114436NIDDK NIH HHS R01 DK120650NIDDK NIH HHS R01 DK132251NIH HHS S10 OD020056NIH HHS S10 OD032447
Abstract
BACKGROUND &
aimsTransformation of stem/progenitor cells has been associated with tumorigenesis in multiple tissues, but stem cells in the stomach have been hard to localize. We therefore aimed to use a combination of several markers to better target oncogenes to gastric stem cells and understand their behavior in the initial stages of gastric tumorigenesis.
methodsMouse models of gastric metaplasia and cancer by targeting stem/progenitor cells were generated and analyzed with techniques including reanalysis of single-cell RNA sequencing and immunostaining. Gastric cancer cell organoids were genetically manipulated with clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) for functional studies. Cell division was determined by bromodeoxyuridine-chasing assay and the assessment of the orientation of the mitotic spindles. Gastric tissues from patients were examined by histopathology and immunostaining.
resultsOncogenic insults lead to expansion of SOX9
conclusionSOX9 marks gastric stem cells and modulates biased symmetric cell division, which appears to be required for the malignant transformation of gastric stem cells.
Indexed as
Proto-Oncogene Proteins p21(ras)Stomach NeoplasmsAnimalsCarcinogenesisCell DivisionCell ProliferationCell Transformation, NeoplasticMiceStem CellsProto-Oncogene Proteins p21(ras)Gastric CancerMetaplasiaMouse ModelNeoplasiaSOX2
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