Mutation of chromatin regulators and focal hotspot alterations characterize human papillomavirus-positive oropharyngeal squamous cell carcinoma

Cancer. 2019 Jul 15;125(14):2423-2434. doi: 10.1002/cncr.32068. Epub 2019 Apr 1.

Abstract

Background: Human papillomavirus (HPV)-associated oropharyngeal cancer is a disease clinically and biologically distinct from smoking-related head and neck squamous cell carcinoma (HNSCC). Despite its rapidly increasing incidence, the mutational landscape of HPV+ oropharyngeal squamous cell carcinoma (OPSCC) remains understudied.

Methods: This article presents the first mutational analysis of the 46 HPV+ OPSCC tumors within the newly expanded cohort of 530 HNSCC tumors from The Cancer Genome Atlas. A separate exome sequencing analysis was also performed for 46 HPV+ OPSCCs matched to their normal lymphocyte controls from the Johns Hopkins University cohort.

Results: There was a strikingly high 33% frequency of mutations within genes associated with chromatin regulation, including mutations in lysine methyltransferase 2C (KMT2C), lysine methyltransferase 2D (KMT2D), nuclear receptor binding SET domain protein 1 (NSD1), CREB binding protein (CREBBP), E1A-associated protein p300 (EP300), and CCCTC-binding factor (CTCF). In addition, the commonly altered genes phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit α (PIK3CA) and fibroblast growth factor receptor 3 (FGFR3) showed distinct domain-specific hotspot mutations in comparison with their HPV- counterparts. PIK3CA showed a uniquely high rate of mutations within the helicase domain, and FGFR3 contained a predominance of hotspot S249C alterations that were not found in HPV- HNSCC.

Conclusions: This analysis represents one of the largest studies to date of HPV+ OPSCC and lends novel insight into the genetic landscape of this biologically distinct disease, including a high rate of mutations in histone- and chromatin-modifying genes, which may offer novel therapeutic targets.

Keywords: The Cancer Genome Atlas (TCGA); epigenetics; exome sequencing; head and neck squamous cell carcinoma; human papillomavirus (HPV); oropharyngeal squamous cell carcinoma.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Aged
  • Chromatin Assembly and Disassembly / genetics*
  • Class I Phosphatidylinositol 3-Kinases / genetics
  • Cohort Studies
  • Exome Sequencing
  • Female
  • Human papillomavirus 16 / immunology*
  • Humans
  • Male
  • Middle Aged
  • Mutation*
  • Oropharyngeal Neoplasms / genetics*
  • Oropharyngeal Neoplasms / pathology
  • Oropharyngeal Neoplasms / virology*
  • Papillomavirus Infections / genetics*
  • Papillomavirus Infections / pathology
  • Papillomavirus Infections / virology
  • Receptor, Fibroblast Growth Factor, Type 3 / genetics
  • Squamous Cell Carcinoma of Head and Neck / genetics*
  • Squamous Cell Carcinoma of Head and Neck / pathology
  • Squamous Cell Carcinoma of Head and Neck / virology*

Substances

  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • FGFR3 protein, human
  • Receptor, Fibroblast Growth Factor, Type 3