Cell-free DNA from germline TP53 mutation carriers reflect cancer-like fragmentation patterns

Nat Commun. 2024 Aug 27;15(1):7386. doi: 10.1038/s41467-024-51529-w.

Abstract

Germline pathogenic TP53 variants predispose individuals to a high lifetime risk of developing multiple cancers and are the hallmark feature of Li-Fraumeni syndrome (LFS). Our group has previously shown that LFS patients harbor shorter plasma cell-free DNA fragmentation; independent of cancer status. To understand the functional underpinning of cfDNA fragmentation in LFS, we conducted a fragmentomic analysis of 199 cfDNA samples from 82 TP53 mutation carriers and 30 healthy TP53-wildtype controls. We find that LFS individuals exhibit an increased prevalence of A/T nucleotides at fragment ends, dysregulated nucleosome positioning at p53 binding sites, and loci-specific changes in chromatin accessibility at development-associated transcription factor binding sites and at cancer-associated open chromatin regions. Machine learning classification resulted in robust differentiation between TP53 mutant versus wildtype cfDNA samples (AUC-ROC = 0.710-1.000) and intra-patient longitudinal analysis of ctDNA fragmentation signal enabled early cancer detection. These results suggest that cfDNA fragmentation may be a useful diagnostic tool in LFS patients and provides an important baseline for cancer early detection.

MeSH terms

  • Adolescent
  • Adult
  • Cell-Free Nucleic Acids* / blood
  • Cell-Free Nucleic Acids* / genetics
  • Child
  • Chromatin / genetics
  • Chromatin / metabolism
  • Circulating Tumor DNA / blood
  • Circulating Tumor DNA / genetics
  • DNA Fragmentation*
  • Early Detection of Cancer
  • Female
  • Germ-Line Mutation*
  • Heterozygote
  • Humans
  • Li-Fraumeni Syndrome* / genetics
  • Machine Learning
  • Male
  • Middle Aged
  • Neoplasms / genetics
  • Neoplasms / pathology
  • Nucleosomes / genetics
  • Nucleosomes / metabolism
  • Tumor Suppressor Protein p53* / genetics
  • Young Adult

Substances

  • Tumor Suppressor Protein p53
  • TP53 protein, human
  • Cell-Free Nucleic Acids
  • Circulating Tumor DNA
  • Chromatin
  • Nucleosomes