Understanding the biological processes of kidney carcinogenesis: an integrative multi-omics approach

Mol Syst Biol. 2024 Dec;20(12):1282-1302. doi: 10.1038/s44320-024-00072-3. Epub 2024 Nov 26.

Abstract

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.

Keywords: Cancer Biology; Genomic Epidemiology; Integrative Multi-omics Analysis; Kidney Cancer; Tumour Microenvironment.

MeSH terms

  • Aging / genetics
  • Carcinogenesis* / genetics
  • DNA Methylation*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Epigenesis, Genetic
  • Epithelial-Mesenchymal Transition* / genetics
  • Gene Expression Regulation, Neoplastic
  • Glutathione S-Transferase pi / genetics
  • Glutathione S-Transferase pi / metabolism
  • Histone-Lysine N-Methyltransferase / genetics
  • Histone-Lysine N-Methyltransferase / metabolism
  • Humans
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / pathology
  • Multiomics
  • Mutation*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcriptome
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • Ubiquitin Thiolesterase

Substances

  • Tumor Suppressor Proteins
  • Glutathione S-Transferase pi
  • BAP1 protein, human
  • GSTP1 protein, human
  • SETD2 protein, human
  • PBRM1 protein, human
  • Transcription Factors
  • Histone-Lysine N-Methyltransferase
  • DNA-Binding Proteins
  • Ubiquitin Thiolesterase