Ricardo Cortez Cardoso Penha, Alexandra Sexton Oates, Sergey Senkin, Hanla A Park, Joshua Atkins, Ivana Holcatova, Anna Hornakova, Slavisa Savic, Simona Ognjanovic, Beata Świątkowska, Jolanta Lissowska, David Zaridze, Anush Mukeria, Vladimir Janout, Amelie Chabrier, Vincent Cahais, Cyrille Cuenin, Ghislaine Scelo, Matthieu Foll, Zdenko Herceg, Paul Brennan, Karl Smith-Byrne, Nicolas Alcala, James D Mckay
{"title":"了解肾癌发生的生物学过程:一种综合的多组学方法。","authors":"Ricardo Cortez Cardoso Penha, Alexandra Sexton Oates, Sergey Senkin, Hanla A Park, Joshua Atkins, Ivana Holcatova, Anna Hornakova, Slavisa Savic, Simona Ognjanovic, Beata Świątkowska, Jolanta Lissowska, David Zaridze, Anush Mukeria, Vladimir Janout, Amelie Chabrier, Vincent Cahais, Cyrille Cuenin, Ghislaine Scelo, Matthieu Foll, Zdenko Herceg, Paul Brennan, Karl Smith-Byrne, Nicolas Alcala, James D Mckay","doi":"10.1038/s44320-024-00072-3","DOIUrl":null,"url":null,"abstract":"<p><p>Biological mechanisms related to cancer development can leave distinct molecular fingerprints in tumours. By leveraging multi-omics and epidemiological information, we can unveil relationships between carcinogenesis processes that would otherwise remain hidden. Our integrative analysis of DNA methylome, transcriptome, and somatic mutation profiles of kidney tumours linked ageing, epithelial-mesenchymal transition (EMT), and xenobiotic metabolism to kidney carcinogenesis. Ageing process was represented by associations with cellular mitotic clocks such as epiTOC2, SBS1, telomere length, and PBRM1 and SETD2 mutations, which ticked faster as tumours progressed. We identified a relationship between BAP1 driver mutations and the epigenetic upregulation of EMT genes (IL20RB and WT1), correlating with increased tumour immune infiltration, advanced stage, and poorer patient survival. We also observed an interaction between epigenetic silencing of the xenobiotic metabolism gene GSTP1 and tobacco use, suggesting a link to genotoxic effects and impaired xenobiotic metabolism. Our pan-cancer analysis showed these relationships in other tumour types. Our study enhances the understanding of kidney carcinogenesis and its relation to risk factors and progression, with implications for other tumour types.</p>","PeriodicalId":18906,"journal":{"name":"Molecular Systems Biology","volume":" ","pages":""},"PeriodicalIF":8.5000,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Understanding the biological processes of kidney carcinogenesis: an integrative multi-omics approach.\",\"authors\":\"Ricardo Cortez Cardoso Penha, Alexandra Sexton Oates, Sergey Senkin, Hanla A Park, Joshua Atkins, Ivana Holcatova, Anna Hornakova, Slavisa Savic, Simona Ognjanovic, Beata Świątkowska, Jolanta Lissowska, David Zaridze, Anush Mukeria, Vladimir Janout, Amelie Chabrier, Vincent Cahais, Cyrille Cuenin, Ghislaine Scelo, Matthieu Foll, Zdenko Herceg, Paul Brennan, Karl Smith-Byrne, Nicolas Alcala, James D Mckay\",\"doi\":\"10.1038/s44320-024-00072-3\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Biological mechanisms related to cancer development can leave distinct molecular fingerprints in tumours. By leveraging multi-omics and epidemiological information, we can unveil relationships between carcinogenesis processes that would otherwise remain hidden. Our integrative analysis of DNA methylome, transcriptome, and somatic mutation profiles of kidney tumours linked ageing, epithelial-mesenchymal transition (EMT), and xenobiotic metabolism to kidney carcinogenesis. Ageing process was represented by associations with cellular mitotic clocks such as epiTOC2, SBS1, telomere length, and PBRM1 and SETD2 mutations, which ticked faster as tumours progressed. We identified a relationship between BAP1 driver mutations and the epigenetic upregulation of EMT genes (IL20RB and WT1), correlating with increased tumour immune infiltration, advanced stage, and poorer patient survival. We also observed an interaction between epigenetic silencing of the xenobiotic metabolism gene GSTP1 and tobacco use, suggesting a link to genotoxic effects and impaired xenobiotic metabolism. Our pan-cancer analysis showed these relationships in other tumour types. Our study enhances the understanding of kidney carcinogenesis and its relation to risk factors and progression, with implications for other tumour types.</p>\",\"PeriodicalId\":18906,\"journal\":{\"name\":\"Molecular Systems Biology\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":8.5000,\"publicationDate\":\"2024-11-26\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular Systems Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1038/s44320-024-00072-3\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Systems Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1038/s44320-024-00072-3","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
Understanding the biological processes of kidney carcinogenesis: an integrative multi-omics approach.
Biological mechanisms related to cancer development can leave distinct molecular fingerprints in tumours. By leveraging multi-omics and epidemiological information, we can unveil relationships between carcinogenesis processes that would otherwise remain hidden. Our integrative analysis of DNA methylome, transcriptome, and somatic mutation profiles of kidney tumours linked ageing, epithelial-mesenchymal transition (EMT), and xenobiotic metabolism to kidney carcinogenesis. Ageing process was represented by associations with cellular mitotic clocks such as epiTOC2, SBS1, telomere length, and PBRM1 and SETD2 mutations, which ticked faster as tumours progressed. We identified a relationship between BAP1 driver mutations and the epigenetic upregulation of EMT genes (IL20RB and WT1), correlating with increased tumour immune infiltration, advanced stage, and poorer patient survival. We also observed an interaction between epigenetic silencing of the xenobiotic metabolism gene GSTP1 and tobacco use, suggesting a link to genotoxic effects and impaired xenobiotic metabolism. Our pan-cancer analysis showed these relationships in other tumour types. Our study enhances the understanding of kidney carcinogenesis and its relation to risk factors and progression, with implications for other tumour types.
期刊介绍:
Systems biology is a field that aims to understand complex biological systems by studying their components and how they interact. It is an integrative discipline that seeks to explain the properties and behavior of these systems.
Molecular Systems Biology is a scholarly journal that publishes top-notch research in the areas of systems biology, synthetic biology, and systems medicine. It is an open access journal, meaning that its content is freely available to readers, and it is peer-reviewed to ensure the quality of the published work.