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This study integrates laser-capture microdissection with multi-omics mini-bulk sequencing to map the oral cancer epigenetic landscape, including chromatin architecture, DNA methylation, H3K27me3, and gene expression. Tumor cells show reorganized chromatin spatial structures and cancer-specific gene interaction networks, with some changes in non-malignant paracancerous tissue. Transformer models classify cancer propensity at individual genome loci, linking conserved structural changes to transcriptomic remodeling, genomic alterations, and methylation reprogramming. 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Molecular Cancer (2024) 23:190 Molecular Cancer  \n[https://doi.org/10.1186/s12943-024-02100-0](https://doi.org/10.1186/s12943-024-02100-0)  \nRESEARCH Open Access  \nUnraveling the key role of chromatin structure in cancer development through epigenetic landscape characterization of oral cancer  \nYue Xue 1†, Lu Liu2†, Ye Zhang3,4,5†, Yueying He 1, Jingyao Wang 1, Zicheng Ma2, Tie-jun Li4,5, Jianyun Zhang4,5*, Yanyi Huang 1,6,7* and Yi Qin Gao 1,2,6*  \nAbstract  \nEpigenetic alterations, such as those in chromatin structure and DNA methylation, have been extensively studied ina number of tumor types. But oral cancer, particularly oral adenocarcinoma, has received far less attention. Here, we combined laser-capture microdissection and muti-omics mini-bulk sequencing to systematically characterize the epigenetic landscape of oral cancer, including chromatin architecture, DNA methylation, H3K27me3 modification, and gene expression. In carcinogenesis, tumor cells exhibit reorganized chromatin spatial structures, including compromised compartment structures and altered gene-gene interaction networks. Notably, some structural alterations are observed in phenotypically non-malignant paracancerous but not in normal cells. We developed transformer models to identify the cancer propensity of individual genome loci, thereby determining the carcinogenic status of each sample. Insights into cancer epigenetic landscapes provide evidence that chromatin reorganization is an important hallmark of oral cancer progression, which is also linked with genomic alterationsand DNA methylation reprogramming. In particular, regions of frequent copy number alternations in cancer  \ncells are associated with strong spatial insulation in both cancer and normal samples. Aberrant methylation reprogramming in oral squamous cell carcinomas is closely related to chromatin structure and H3K27me3 signals, which are further influenced by intrinsic sequence properties. Our findings indicate that structural changes are both significant and conserved in two distinct types of oral cancer, closely linked to transcriptomic alterations and cancer development. Notably, the structural changes remain markedly evident in oral adenocarcinoma despite the considerably lower incidence of genomic copy number alterations and lesser extent of methylation alterations compared to squamous cell carcinoma. We expect that the comprehensive analysis of epigenetic reprogramming of different types and subtypes of primary oral tumors can provide additional guidance to the design of novel detection and therapy for oral cancer.  \n†Yue Xue, Lu Liu andYe Zhang contributed equally to this work.  \n*Correspondence:  \nJianyun Zhang [jianyunz0509@aliyun.com](jianyunz0509@aliyun.com)[ ](jianyunz0509@aliyun.com)Yanyi Huang [yanyi@pku.edu.cn](yanyi@pku.edu.cn)[ ](yanyi@pku.edu.cn)Yi Qin Gao [gaoyq@pku.edu.cn](gaoyq@pku.edu.cn)  \nFull list of author information is available at the end of the article  \n© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit [http://](http://)[ ]","cbCaic6VwRwaVdrE","https://ap.wps.com/l/cbCaic6VwRwaVdrE","pdf",15134599,24,"English","# Abstract\n# Introduction\n## Epigenetic and genetic alterations in oral cancers","[{\"question\":\"Do structural chromatin changes occur only in malignant cells?\",\"answer\":\"Some structural alterations are observed in phenotypically non-malignant paracancerous cells, while not appearing in normal cells.\"}]","Unraveling the key role of chromatin structure in cancer development through epigenetic landscape characterization of oral cancer | PDF",1789992480]