FOXM1 drives HPV+ HNSCC sensitivity to WEE1 inhibition

Proc Natl Acad Sci U S A. 2020 Nov 10;117(45):28287-28296. doi: 10.1073/pnas.2013921117. Epub 2020 Oct 22.

Abstract

Head and neck squamous cell carcinoma (HNSCC) associated with high-risk human papilloma virus (HPV) infection is a growing clinical problem. The WEE1 kinase inhibitor AZD1775 (WEE1i) overrides cell cycle checkpoints and is being studied in HNSCC regimens. We show that the HPV16 E6/E7 oncoproteins sensitize HNSCC cells to single-agent WEE1i treatment through activation of a FOXM1-CDK1 circuit that drives mitotic gene expression and DNA damage. An isogenic cell system indicated that E6 largely accounts for these phenotypes in ways that extend beyond p53 inactivation. A targeted genomic analysis implicated FOXM1 signaling downstream of E6/E7 expression and analyses of primary tumors and The Cancer Genome Atlas (TCGA) data revealed an activated FOXM1-directed promitotic transcriptional signature in HPV+ versus HPV- HNSCCs. Finally, we demonstrate the causality of FOXM1 in driving WEE1i sensitivity. These data suggest that elevated basal FOXM1 activity predisposes HPV+ HNSCC to WEE1i-induced toxicity and provide mechanistic insights into WEE1i and HPV+ HNSCC therapies.

Keywords: AZD1775; FOXM1; HPV16; WEE1; head and neck cancer.

Publication types

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

MeSH terms

  • CDC2 Protein Kinase / metabolism
  • Cell Cycle Checkpoints
  • Cell Cycle Proteins / drug effects*
  • Cell Cycle Proteins / metabolism
  • Cell Line, Tumor
  • DNA Damage / drug effects
  • Forkhead Box Protein M1 / metabolism*
  • Head and Neck Neoplasms
  • Humans
  • Oncogene Proteins, Viral / metabolism
  • Papillomavirus E7 Proteins / metabolism
  • Papillomavirus Infections / drug therapy*
  • Protein-Tyrosine Kinases / drug effects*
  • Protein-Tyrosine Kinases / metabolism
  • Pyrazoles / antagonists & inhibitors*
  • Pyrimidinones / antagonists & inhibitors*
  • Repressor Proteins / metabolism
  • Squamous Cell Carcinoma of Head and Neck / drug therapy*
  • Up-Regulation

Substances

  • Cell Cycle Proteins
  • E6 protein, Human papillomavirus type 16
  • FOXM1 protein, human
  • Forkhead Box Protein M1
  • Oncogene Proteins, Viral
  • Papillomavirus E7 Proteins
  • Pyrazoles
  • Pyrimidinones
  • Repressor Proteins
  • Protein-Tyrosine Kinases
  • WEE1 protein, human
  • CDC2 Protein Kinase
  • CDK1 protein, human
  • adavosertib