Multiregion human bladder cancer sequencing reveals tumour evolution, bladder cancer phenotypes and implications for targeted therapy

J Pathol. 2019 Jun;248(2):230-242. doi: 10.1002/path.5250. Epub 2019 Mar 18.

Abstract

We present an evolutionary analysis of the relative time of genetic events underlying tumorigenesis in human bladder cancers from 10 whole cystectomy specimens using multiregional whole-exome sequencing. We timed bladder cancer drivers, mutational signatures, ploidy and copy number alterations, provided evidence for kataegis and correlated alterations with tumour areas and histological phenotypes. We found that: (1) heterogeneous tumour areas/phenotypes had distinct driver mutations, (2) papillary-invasive tumours divided early into two parallel evolving branches and (3) parallel evolution of subclonal driver mutations occurred. APOBEC mutational signatures were found to be very early events, active in carcinoma in situ, and often remained a dominant source of mutations throughout tumour evolution. Genetic progression from carcinoma in situ followed driver mutations in NA13/FAT1, ZBTB7B or EP300/USP28/KMT2D. Our results point towards a more diverse mutational trajectory of bladder tumorigenesis and underpin the importance of timing of mutational processes and clonal architecture in bladder cancer as important aspects for successful prognostication and therapy. Copyright © 2019 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

Keywords: bladder cancer; kataegis; phylogenetic analysis; tumour evolution; tumour heterogeneity; tumour phenotype.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Biomarkers, Tumor / genetics*
  • Carcinoma / drug therapy
  • Carcinoma / genetics*
  • Carcinoma / pathology
  • Carcinoma / surgery
  • Carcinoma in Situ / drug therapy
  • Carcinoma in Situ / genetics*
  • Carcinoma in Situ / pathology
  • Carcinoma in Situ / surgery
  • Cystectomy
  • DNA Copy Number Variations
  • Disease Progression
  • Exome Sequencing*
  • Female
  • Gene Dosage
  • Genetic Heterogeneity*
  • Genetic Predisposition to Disease
  • Humans
  • Male
  • Middle Aged
  • Molecular Targeted Therapy
  • Mutation
  • Neoplasm Invasiveness
  • Phenotype
  • Ploidies
  • Precision Medicine
  • Time Factors
  • Transcriptome*
  • Urinary Bladder Neoplasms / drug therapy
  • Urinary Bladder Neoplasms / genetics*
  • Urinary Bladder Neoplasms / pathology
  • Urinary Bladder Neoplasms / surgery

Substances

  • Biomarkers, Tumor