A comparison of isolated circulating tumor cells and tissue biopsies using whole-genome sequencing in prostate cancer

Oncotarget. 2015 Dec 29;6(42):44781-93. doi: 10.18632/oncotarget.6330.

Abstract

Previous studies have demonstrated focal but limited molecular similarities between circulating tumor cells (CTCs) and biopsies using isolated genetic assays. We hypothesized that molecular similarity between CTCs and tissue exists at the single cell level when characterized by whole genome sequencing (WGS). By combining the NanoVelcro CTC Chip with laser capture microdissection (LCM), we developed a platform for single-CTC WGS. We performed this procedure on CTCs and tissue samples from a patient with advanced prostate cancer who had serial biopsies over the course of his clinical history. We achieved 30X depth and ≥ 95% coverage. Twenty-nine percent of the somatic single nucleotide variations (SSNVs) identified were founder mutations that were also identified in CTCs. In addition, 86% of the clonal mutations identified in CTCs could be traced back to either the primary or metastatic tumors. In this patient, we identified structural variations (SVs) including an intrachromosomal rearrangement in chr3 and an interchromosomal rearrangement between chr13 and chr15. These rearrangements were shared between tumor tissues and CTCs. At the same time, highly heterogeneous short structural variants were discovered in PTEN, RB1, and BRCA2 in all tumor and CTC samples. Using high-quality WGS on single-CTCs, we identified the shared genomic alterations between CTCs and tumor tissues. This approach yielded insight into the heterogeneity of the mutational landscape of SSNVs and SVs. It may be possible to use this approach to study heterogeneity and characterize the biological evolution of a cancer during the course of its natural history.

Keywords: cancer heterogeneity; circulating tumor cell; liquid biopsy; prostate cancer; whole genome sequencing.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Base Sequence
  • Biomarkers, Tumor / genetics*
  • Biopsy
  • Cell Separation
  • Chromosomes, Human
  • DNA Mutational Analysis
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation, Neoplastic
  • Gene Rearrangement
  • Genetic Predisposition to Disease
  • Genome-Wide Association Study
  • Genomics / methods*
  • Humans
  • Laser Capture Microdissection
  • Liver Neoplasms / genetics
  • Liver Neoplasms / secondary
  • Male
  • Molecular Sequence Data
  • Mutation
  • Nanotechnology
  • Neoplastic Cells, Circulating / chemistry*
  • Neoplastic Cells, Circulating / pathology
  • Oligonucleotide Array Sequence Analysis
  • Phenotype
  • Polymorphism, Single Nucleotide
  • Predictive Value of Tests
  • Prostatic Neoplasms / blood
  • Prostatic Neoplasms / genetics*
  • Prostatic Neoplasms / pathology
  • Prostatic Neoplasms / therapy
  • Time Factors

Substances

  • Biomarkers, Tumor