Clonal phylogenies inferred from bulk, single cell, and spatial transcriptomic analysis of epithelial cancers

PLoS One. 2025 Jan 3;20(1):e0316475. doi: 10.1371/journal.pone.0316475. eCollection 2025.

Abstract

Epithelial cancers are typically heterogeneous with primary prostate cancer being a typical example of histological and genomic variation. Prior studies of primary prostate cancer tumour genetics revealed extensive inter and intra-patient genomic tumour heterogeneity. Recent advances in machine learning have enabled the inference of ground-truth genomic single-nucleotide and copy number variant status from transcript data. While these inferred SNV and CNV states can be used to resolve clonal phylogenies, however, it is still unknown how faithfully transcript-based tumour phylogenies reconstruct ground truth DNA-based tumour phylogenies. We sought to study the accuracy of inferred-transcript to recapitulate DNA-based tumour phylogenies. We first performed in-silico comparisons of inferred and directly resolved SNV and CNV status, from single cancer cells, from three different cell lines. We found that inferred SNV phylogenies accurately recapitulate DNA phylogenies (entanglement = 0.097). We observed similar results in iCNV and CNV based phylogenies (entanglement = 0.11). Analysis of published prostate cancer DNA phylogenies and inferred CNV, SNV and transcript based phylogenies demonstrated phylogenetic concordance. Finally, a comparison of pseudo-bulked spatial transcriptomic data to adjacent sections with WGS data also demonstrated recapitulation of ground truth (entanglement = 0.35). These results suggest that transcript-based inferred phylogenies recapitulate conventional genomic phylogenies. Further work will need to be done to increase accuracy, genomic, and spatial resolution.

MeSH terms

  • Cell Line, Tumor
  • Clone Cells
  • DNA Copy Number Variations*
  • Gene Expression Profiling / methods
  • Humans
  • Male
  • Phylogeny*
  • Polymorphism, Single Nucleotide
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / pathology
  • Single-Cell Analysis* / methods
  • Transcriptome

Grants and funding

This study was financially supported by Cancer Research UK (https://www.cancerresearchuk.org/) in the form of a grant (C57899/A25812) received by AL. This study was also financially supported by the Oxford NIHR Biomedical Research Centre Surgical Innovation & Evaluation (https://oxfordbrc.nihr.ac.uk/research-themes/surgical-innovation-technology-and-evaluation/) in the form of an award received by AL. This study was also financially supported by Academy of Finland (https://www.aka.fi/) in the form of a grant (360763) received by AE. This study was also financially supported by Cancer Society of Finland (https://www.cancersociety.fi/) in the form of a grant (63-6403) received by AE. This study was also financially supported by Sigrid Jusélius Foundation (https://www.sigridjuselius.fi/) in the form of a grant (230024) received by AE. This study was also financially supported by Instrumentariumin Tiedesäätiö (https://www.instrufoundation.fi/) in the form of a grant (240003) received by AE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.