Spatiotemporal genomic profiling of intestinal metaplasia reveals clonal dynamics of gastric cancer progression
Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin r...
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| Published in | Cancer cell Vol. 41; no. 12; pp. 2019 - 2037.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
11.12.2023
Cell Press |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1535-6108 1878-3686 1878-3686 |
| DOI | 10.1016/j.ccell.2023.10.004 |
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| Abstract | Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (ARID1A) and intestinal homeostasis (SOX9). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types, ARID1A mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception.
[Display omitted]
•Genomic profiling reveals 26 intestinal metaplasia (IM) driver genes including SOX9•IM lineage heterogeneity harbors a stem-cell subpopulation linked to malignancy•IM molecular subtypes are associated with inflammation and microbial communities•Genomic-clinical models improve identification of IMs at risk of GC progression
Intestinal metaplasia (IM) is a pre-malignant condition linked to gastric cancer (GC). Huang et al. analyze a large prospective IM cohort, identifying driver genes, stem cell populations linked to GC, and molecular subtypes associated with inflammation and oral microbes. These results facilitate the use of genomics in GC precision prevention. |
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| AbstractList | Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (
ARID1A
) and intestinal homeostasis (
SOX9
). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types,
ARID1A
mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception.
•
Genomic profiling reveals 26 intestinal metaplasia (IM) driver genes including
SOX9
•
IM lineage heterogeneity harbors a stem-cell subpopulation linked to malignancy
•
IM molecular subtypes are associated with inflammation and microbial communities
•
Genomic-clinical models improve identification of IMs at risk of GC progression
Intestinal metaplasia (IM) is a pre-malignant condition linked to gastric cancer (GC). Huang et al. analyze a large prospective IM cohort, identifying driver genes, stem cell populations linked to GC, and molecular subtypes associated with inflammation and oral microbes. These results facilitate the use of genomics in GC precision prevention. Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (ARID1A) and intestinal homeostasis (SOX9). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types, ARID1A mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception. [Display omitted] •Genomic profiling reveals 26 intestinal metaplasia (IM) driver genes including SOX9•IM lineage heterogeneity harbors a stem-cell subpopulation linked to malignancy•IM molecular subtypes are associated with inflammation and microbial communities•Genomic-clinical models improve identification of IMs at risk of GC progression Intestinal metaplasia (IM) is a pre-malignant condition linked to gastric cancer (GC). Huang et al. analyze a large prospective IM cohort, identifying driver genes, stem cell populations linked to GC, and molecular subtypes associated with inflammation and oral microbes. These results facilitate the use of genomics in GC precision prevention. Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (ARID1A) and intestinal homeostasis (SOX9). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types, ARID1A mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception. Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (ARID1A) and intestinal homeostasis (SOX9). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types, ARID1A mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception.Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric samples (1,152 IMs) across 692 subjects from a prospective 10-year study, we identify 26 IM driver genes in diverse pathways including chromatin regulation (ARID1A) and intestinal homeostasis (SOX9). Single-cell and spatial profiles highlight changes in tissue ecology and IM lineage heterogeneity, including an intestinal stem-cell dominant cellular compartment linked to early malignancy. Expanded transcriptome profiling reveals expression-based molecular subtypes of IM associated with incomplete histology, antral/intestinal cell types, ARID1A mutations, inflammation, and microbial communities normally associated with the healthy oral tract. We demonstrate that combined clinical-genomic models outperform clinical-only models in predicting IMs likely to transform to GC. By highlighting strategies for accurately identifying IM patients at high GC risk and a role for microbial dysbiosis in IM progression, our results raise opportunities for GC precision prevention and interception. |
| Author | Lee, Minghui Yang, Wei Lyn Tan, Angie Lay Keng Lian, Benedict Shi Xiang Ong, Xuewen Chua, Joy Shijia Zhu, Feng Sheng, Taotao Lesluyes, Tom Yeoh, Khay Guan Ang, Tiing Leong Tsao, Stephen Kin Kwok So, Jimmy Bok Yan Khor, Christopher Ramnarayanan, Kalpana Smoot, Duane Gotoda, Takuji Uchihara, Tomoyuki Srivastava, Supriya Huang, Kie Kyon Tay, Su Ting Ho, Shamaine Wei Ting Teh, Ming Sundar, Raghav Chong, Roxanne Hui Heng Tan, Patrick Lau, Louis Ho Shing Kim, Hyun Soo Ma, Haoran Ashktorab, Hassan Van Loo, Peter Lee, Jonathan Wei Jie Chung, Hyunsoo |
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169857, Singapore – sequence: 6 givenname: Feng surname: Zhu fullname: Zhu, Feng organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 7 givenname: Taotao surname: Sheng fullname: Sheng, Taotao organization: Genome Institute of Singapore, Agency for Science, Technology and Research, Singapore, Singapore – sequence: 8 givenname: Supriya surname: Srivastava fullname: Srivastava, Supriya organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 9 givenname: Su Ting surname: Tay fullname: Tay, Su Ting organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 10 givenname: Raghav surname: Sundar fullname: Sundar, Raghav organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 11 givenname: Angie Lay Keng surname: Tan fullname: Tan, Angie Lay Keng organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 12 givenname: Xuewen surname: Ong fullname: Ong, Xuewen organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 13 givenname: Minghui surname: Lee fullname: Lee, Minghui organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 14 givenname: Shamaine Wei Ting surname: Ho fullname: Ho, Shamaine Wei Ting organization: Genome Institute of Singapore, Agency for Science, Technology and Research, Singapore, Singapore – sequence: 15 givenname: Tom surname: Lesluyes fullname: Lesluyes, Tom organization: The Francis Crick Institute, London, UK – sequence: 16 givenname: Hassan surname: Ashktorab fullname: Ashktorab, Hassan organization: Department of Medicine, Howard University, Washington, DC, USA – sequence: 17 givenname: Duane surname: Smoot fullname: Smoot, Duane organization: Department of Internal Medicine, Meharry Medical College, Nashville, TN, USA – sequence: 18 givenname: Peter surname: Van Loo fullname: Van Loo, Peter organization: The Francis Crick Institute, London, UK – sequence: 19 givenname: Joy Shijia surname: Chua fullname: Chua, Joy Shijia organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 20 givenname: Kalpana surname: Ramnarayanan fullname: Ramnarayanan, Kalpana organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore – sequence: 21 givenname: Louis Ho Shing surname: Lau fullname: Lau, Louis Ho Shing organization: Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, Hong Kong – sequence: 22 givenname: Takuji surname: Gotoda fullname: Gotoda, Takuji organization: Division of Gastroenterology and Hepatology, Department of Medicine, Nihon University School of Medicine, Tokyo, Japan – sequence: 23 givenname: Hyun Soo surname: Kim fullname: Kim, Hyun Soo organization: Department of Internal Medicine, Yonsei University Wonju College of Medicine, Seoul, Korea – sequence: 24 givenname: Tiing Leong surname: Ang fullname: Ang, Tiing Leong organization: Department of Gastroenterology & Hepatology, Changi General Hospital, Singapore 529889, Singapore – sequence: 25 givenname: Christopher surname: Khor fullname: Khor, Christopher organization: Department of Gastroenterology & Hepatology, Singapore General Hospital, Singapore 169854, Singapore – sequence: 26 givenname: Jonathan Wei Jie surname: Lee fullname: Lee, Jonathan Wei Jie organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 27 givenname: Stephen Kin Kwok surname: Tsao fullname: Tsao, Stephen Kin Kwok organization: Department of Gastroenterology & Hepatology, Tan Tock Seng Hospital, Singapore 308433, Singapore – sequence: 28 givenname: Wei Lyn surname: Yang fullname: Yang, Wei Lyn organization: Department of Gastroenterology & Hepatology, Tan Tock Seng Hospital, Singapore 308433, Singapore – sequence: 29 givenname: Ming surname: Teh fullname: Teh, Ming organization: Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 30 givenname: Hyunsoo surname: Chung fullname: Chung, Hyunsoo email: h.chung@snu.ac.kr organization: Department of Internal Medicine, Seoul National University Hospital, Seoul, Korea – sequence: 31 givenname: Jimmy Bok Yan surname: So fullname: So, Jimmy Bok Yan email: jimmyso@nus.edu.sg organization: Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 32 givenname: Khay Guan surname: Yeoh fullname: Yeoh, Khay Guan email: mdcykg@nus.edu.sg organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore – sequence: 33 givenname: Patrick orcidid: 0000-0002-0179-8048 surname: Tan fullname: Tan, Patrick email: gmstanp@duke-nus.edu.sg organization: Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore 169857, Singapore |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37890493$$D View this record in MEDLINE/PubMed |
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| Keywords | targeted DNA sequencing single-cell sequencing cancer screening gastric cancer transcriptome sequencing intestinal metaplasia spatial transcriptomics cell-of-origin pre-cancer |
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| Snippet | Intestinal metaplasia (IM) is a pre-malignant condition of the gastric mucosa associated with increased gastric cancer (GC) risk. Analyzing 1,256 gastric... |
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| SubjectTerms | cancer screening cell-of-origin gastric cancer Gastric Mucosa - pathology Genomics Humans intestinal metaplasia Metaplasia - genetics pre-cancer Precancerous Conditions - genetics Prospective Studies single-cell sequencing spatial transcriptomics Stomach Neoplasms - genetics Stomach Neoplasms - metabolism targeted DNA sequencing transcriptome sequencing |
| Title | Spatiotemporal genomic profiling of intestinal metaplasia reveals clonal dynamics of gastric cancer progression |
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