Analysis of a cell-free DNA-based cancer screening cohort links fragmentomic profiles, nuclease levels, and plasma DNA concentrations

Genome Res. 2024 Nov 27:gr.279667.124. doi: 10.1101/gr.279667.124. Online ahead of print.

Abstract

The concentration of circulating cell-free DNA (cfDNA) in plasma is an important determinant of the robustness of liquid biopsies. However, biological mechanisms that lead to inter-individual differences in cfDNA concentrations remain unexplored. The concentration of plasma cfDNA is governed by an interplay between its release and clearance. We hypothesize that cfDNA clearance by nucleases might be one mechanism that contributes towards inter-individual variations in cfDNA concentrations. We performed fragmentomic analysis of the plasma cfDNA from 862 healthy individuals, with a cfDNA concentration range of 1.61 - 41.01 ng/mL. We observed an increase in large DNA fragments (231-600 bp), a decreased frequencies of shorter DNA fragments (20-160 bp), and an increased frequency of G-end motifs with increasing cfDNA concentrations. End motif deconvolution analysis revealed a decreased contribution of DNASE1L3 and DFFB in subjects with higher cfDNA concentration. The five subjects with the highest plasma DNA concentration (top 0.58%) had aberrantly decreased levels of DNASE1L3 protein in plasma. The cfDNA concentration could be inferred from the fragmentomic profile through machine learning, and was well correlated to the measured cfDNA concentration. Such an approach could infer the fractional DNA concentration from particular tissue types, such as the fetal and tumor fraction. This work shows that individuals with different cfDNA concentrations were associated with characteristic fragmentomic patterns of the cfDNA pool; and that nuclease-mediated clearance of DNA is a key parameter that affects cfDNA concentration. Understanding these mechanisms has facilitated the enhanced measurement of cfDNA species of clinical interest, including circulating fetal and tumor DNA.