Circulating tumor extracellular vesicles to monitor metastatic prostate cancer genomics and transcriptomic evolution

Cancer Cell. 2024 Jul 8;42(7):1301-1312.e7. doi: 10.1016/j.ccell.2024.06.003.

Abstract

Extracellular vesicles (EVs) secreted by tumors are abundant in plasma, but their potential for interrogating the molecular features of tumors through multi-omic profiling remains widely unexplored. Genomic and transcriptomic profiling of circulating EV-DNA and EV-RNA isolated from in vitro and in vivo models of metastatic prostate cancer (mPC) reveal a high contribution of tumor material to EV-loaded DNA/RNA, validating the findings in two cohorts of longitudinal plasma samples collected from patients during androgen receptor signaling inhibitor (ARSI) or taxane-based therapy. EV-DNA genomic features recapitulate matched-patient biopsies and circulating tumor DNA (ctDNA) and associate with clinical progression. We develop a novel approach to enable transcriptomic profiling of EV-RNA (RExCuE). We report how the transcriptome of circulating EVs is enriched for tumor-associated transcripts, captures certain patient and tumor features, and reflects on-therapy tumor adaptation changes. Altogether, we show that EV profiling enables longitudinal transcriptomic and genomic profiling of mPC in liquid biopsy.

Keywords: biomarkers; extracellular vesicles; liquid biopsy; prostate cancer; transcriptomics.

MeSH terms

  • Animals
  • Biomarkers, Tumor / blood
  • Biomarkers, Tumor / genetics
  • Cell Line, Tumor
  • Circulating Tumor DNA / blood
  • Circulating Tumor DNA / genetics
  • Extracellular Vesicles* / genetics
  • Extracellular Vesicles* / metabolism
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Neoplastic
  • Genomics* / methods
  • Humans
  • Liquid Biopsy / methods
  • Male
  • Mice
  • Neoplasm Metastasis
  • Prostatic Neoplasms* / blood
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / pathology
  • Transcriptome*

Substances

  • Biomarkers, Tumor
  • Circulating Tumor DNA