Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset

Abstract Background Understanding cellular diversity throughout the body is essential for elucidating the complex functions of biological systems. Recently, large-scale single-cell omics datasets, known as omics atlases, have become available. These atlases encompass data from diverse tissues and ce...

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Main Authors: Daigo Okada, Jianshen Zhu, Kan Shota, Yuuki Nishimura, Kazuya Haraguchi
Format: Article
Language:English
Published: BMC 2025-04-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11614-w
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author Daigo Okada
Jianshen Zhu
Kan Shota
Yuuki Nishimura
Kazuya Haraguchi
author_facet Daigo Okada
Jianshen Zhu
Kan Shota
Yuuki Nishimura
Kazuya Haraguchi
author_sort Daigo Okada
collection DOAJ
description Abstract Background Understanding cellular diversity throughout the body is essential for elucidating the complex functions of biological systems. Recently, large-scale single-cell omics datasets, known as omics atlases, have become available. These atlases encompass data from diverse tissues and cell-types, providing insights into the landscape of cell-type-specific gene expression. However, the isolated effect of the tissue environment has not been thoroughly investigated. Evaluating this isolated effect is challenging due to statistical confounding with cell-type effects, which arises from the highly limited subset of tissue-cell-type combinations that are biologically realized compared to the vast number of theoretical possibilities. Results This study introduces a novel data analysis framework, named the Combinatorial Sub-dataset Extraction for Confounding Reduction (COSER), which addresses statistical confounding by using graph theory to enumerate appropriate sub-datasets. COSER enables the assessment of isolated effects of discrete variables in single cells. Applying COSER to the Tabula Muris Senis single-cell transcriptome atlas, we characterized the isolated impact of tissue environments. Our findings demonstrate that some genes are markedly affected by the tissue environment, particularly in modulating intercellular diversity in immune responses and their age-related changes. Conclusion COSER provides a robust, general-purpose framework for evaluating the isolated effects of discrete variables from large-scale data mining. This approach reveals critical insights into the interplay between tissue environments and gene expression.
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spelling doaj-art-c68ea5cd482d4414939465741b2b06802025-08-20T02:55:31ZengBMCBMC Genomics1471-21642025-04-0126111410.1186/s12864-025-11614-wSystematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas datasetDaigo Okada0Jianshen Zhu1Kan Shota2Yuuki Nishimura3Kazuya Haraguchi4Center for Genomic Medicine, Graduate School of Medicine, Kyoto UniversityDiscrete Mathematics Laboratory, Applied Mathematics and Physics Course, Graduate School of Informatics, Kyoto UniversityDiscrete Mathematics Laboratory, Applied Mathematics and Physics Course, Graduate School of Informatics, Kyoto UniversityDiscrete Mathematics Laboratory, Applied Mathematics and Physics Course, Graduate School of Informatics, Kyoto UniversityDiscrete Mathematics Laboratory, Applied Mathematics and Physics Course, Graduate School of Informatics, Kyoto UniversityAbstract Background Understanding cellular diversity throughout the body is essential for elucidating the complex functions of biological systems. Recently, large-scale single-cell omics datasets, known as omics atlases, have become available. These atlases encompass data from diverse tissues and cell-types, providing insights into the landscape of cell-type-specific gene expression. However, the isolated effect of the tissue environment has not been thoroughly investigated. Evaluating this isolated effect is challenging due to statistical confounding with cell-type effects, which arises from the highly limited subset of tissue-cell-type combinations that are biologically realized compared to the vast number of theoretical possibilities. Results This study introduces a novel data analysis framework, named the Combinatorial Sub-dataset Extraction for Confounding Reduction (COSER), which addresses statistical confounding by using graph theory to enumerate appropriate sub-datasets. COSER enables the assessment of isolated effects of discrete variables in single cells. Applying COSER to the Tabula Muris Senis single-cell transcriptome atlas, we characterized the isolated impact of tissue environments. Our findings demonstrate that some genes are markedly affected by the tissue environment, particularly in modulating intercellular diversity in immune responses and their age-related changes. Conclusion COSER provides a robust, general-purpose framework for evaluating the isolated effects of discrete variables from large-scale data mining. This approach reveals critical insights into the interplay between tissue environments and gene expression.https://doi.org/10.1186/s12864-025-11614-wSingle cell RNA-seqEffect of tissue environmentGraph theoryMaximal biclique enumeration
spellingShingle Daigo Okada
Jianshen Zhu
Kan Shota
Yuuki Nishimura
Kazuya Haraguchi
Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
BMC Genomics
Single cell RNA-seq
Effect of tissue environment
Graph theory
Maximal biclique enumeration
title Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
title_full Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
title_fullStr Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
title_full_unstemmed Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
title_short Systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single-cell RNA-seq atlas dataset
title_sort systematic evaluation of the isolated effect of tissue environment on the transcriptome using a single cell rna seq atlas dataset
topic Single cell RNA-seq
Effect of tissue environment
Graph theory
Maximal biclique enumeration
url https://doi.org/10.1186/s12864-025-11614-w
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