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DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity

Abstract:

Background: Epigenetic modifications in mammalian DNA are commonly manifested by DNA methylation. In the stomach, altered DNA methylation patterns have been observed following chronic Helicobacter pylori infections and in gastric cancer. In the context of epigenetic regulation, the regional nature of the stomach has been rarely considered in detail.

Results: Here, we establish gastric mucosa derived primary cell cultures as a reliable source of native human epithelium. We describe the DNA methylation landscape across the phenotypically different regions of the healthy human stomach, i.e., antrum, corpus, fundus together with the corresponding transcriptomes. We show that stable regional DNA methylation differences translate to a limited extent into regulation of the transcriptomic phenotype, indicating a largely permissive epigenetic regulation. We identify a small number of transcription factors with novel region-specific activity and likely epigenetic impact in the stomach, including GATA4, IRX5, IRX2, PDX1 and CDX2. Detailed analysis of the Wnt pathway reveals differential regulation along the craniocaudal axis, which involves non-canonical Wnt signaling in determining cell fate in the proximal stomach. By extending our analysis to pre-neoplastic lesions and gastric cancers, we conclude that epigenetic dysregulation characterizes intestinal metaplasia as a founding basis for functional changes in gastric cancer. We present insights into the dynamics of DNA methylation across anatomical regions of the healthy stomach and patterns of its change in disease. Finally, our study provides a well-defined resource of regional stomach transcription and epigenetics.

Publication status:
Published
Peer review status:
Peer reviewed

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Files:
Publisher copy:
10.1186/s13148-022-01406-4

Authors


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Institution:
University of Oxford
Division:
MSD
Department:
NDM
Sub department:
Oxford Ludwig Institute
Role:
Author
ORCID:
0000-0001-6013-7154


Publisher:
BioMed Central
Journal:
Clinical Epigenetics More from this journal
Volume:
14
Issue:
193
Publication date:
2022-12-30
Acceptance date:
2022-12-13
DOI:
EISSN:
1868-7083
ISSN:
1868-7075
Pmid:
36585699


Language:
English
Keywords:
Pubs id:
1319292
Local pid:
pubs:1319292
Deposit date:
2023-01-17

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