Whole-Genome Sequencing Reveals Diverse Models of Structural Variations in Esophageal Squamous Cell Carcinoma

Am J Hum Genet. 2016 Feb 4;98(2):256-74. doi: 10.1016/j.ajhg.2015.12.013. Epub 2016 Jan 28.

Abstract

Comprehensive identification of somatic structural variations (SVs) and understanding their mutational mechanisms in cancer might contribute to understanding biological differences and help to identify new therapeutic targets. Unfortunately, characterization of complex SVs across the whole genome and the mutational mechanisms underlying esophageal squamous cell carcinoma (ESCC) is largely unclear. To define a comprehensive catalog of somatic SVs, affected target genes, and their underlying mechanisms in ESCC, we re-analyzed whole-genome sequencing (WGS) data from 31 ESCCs using Meerkat algorithm to predict somatic SVs and Patchwork to determine copy-number changes. We found deletions and translocations with NHEJ and alt-EJ signature as the dominant SV types, and 16% of deletions were complex deletions. SVs frequently led to disruption of cancer-associated genes (e.g., CDKN2A and NOTCH1) with different mutational mechanisms. Moreover, chromothripsis, kataegis, and breakage-fusion-bridge (BFB) were identified as contributing to locally mis-arranged chromosomes that occurred in 55% of ESCCs. These genomic catastrophes led to amplification of oncogene through chromothripsis-derived double-minute chromosome formation (e.g., FGFR1 and LETM2) or BFB-affected chromosomes (e.g., CCND1, EGFR, ERBB2, MMPs, and MYC), with approximately 30% of ESCCs harboring BFB-derived CCND1 amplification. Furthermore, analyses of copy-number alterations reveal high frequency of whole-genome duplication (WGD) and recurrent focal amplification of CDCA7 that might act as a potential oncogene in ESCC. Our findings reveal molecular defects such as chromothripsis and BFB in malignant transformation of ESCCs and demonstrate diverse models of SVs-derived target genes in ESCCs. These genome-wide SV profiles and their underlying mechanisms provide preventive, diagnostic, and therapeutic implications for ESCCs.

Keywords: ESCC; breakage-fusion-bridge; chromothripsis; structural variation; whole-genome duplication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinoma, Squamous Cell / genetics*
  • Cell Line
  • Cyclin D1 / genetics
  • DNA Copy Number Variations
  • ErbB Receptors / genetics
  • Esophageal Neoplasms / genetics*
  • Esophageal Squamous Cell Carcinoma
  • Gene Deletion
  • Gene Rearrangement
  • Genes, p16
  • Genetic Association Studies / methods*
  • Genetic Variation*
  • Genome, Human
  • Genomics
  • Humans
  • In Situ Hybridization, Fluorescence
  • Receptor, ErbB-2 / genetics
  • Receptor, Fibroblast Growth Factor, Type 1 / genetics
  • Receptor, Notch1 / genetics
  • Reproducibility of Results
  • Sequence Analysis, RNA
  • Translocation, Genetic

Substances

  • CCND1 protein, human
  • NOTCH1 protein, human
  • Receptor, Notch1
  • Cyclin D1
  • EGFR protein, human
  • ERBB2 protein, human
  • ErbB Receptors
  • FGFR1 protein, human
  • Receptor, ErbB-2
  • Receptor, Fibroblast Growth Factor, Type 1