EZH2-mediated upregulation of ROS1 oncogene promotes oral cancer metastasis

Oncogene. 2017 Nov 23;36(47):6542-6554. doi: 10.1038/onc.2017.262. Epub 2017 Jul 31.

Abstract

Current anti-epidermal growth factor receptor (EGFR) therapy for oral cancer does not provide satisfactory efficacy due to drug resistance or reduced EGFR level. As an alternative candidate target for therapy, here we identified an oncogene, ROS1, as an important driver for oral squamous cell carcinoma (OSCC) metastasis. Among tumors from 188 oral cancer patients, upregulated ROS1 expression strongly correlated with metastasis to lung and lymph nodes. Mechanistic studies uncover that the activated ROS1 results from highly expressed ROS1 gene instead of gene rearrangement, a phenomenon distinct from other cancers. Our data further reveal a novel mechanism that reduced histone methyltransferase EZH2 leads to a lower trimethylation of histone H3 lysine 27 suppressive modification, relaxes chromatin, and promotes the accessibility of the transcription factor STAT1 to the enhancer and the intron regions of ROS1 target genes, CXCL1 and GLI1, for upregulating their expressions. Down-regulation of ROS1 in highly invasive OSCC cells, nevertheless, reduces cell proliferation and inhibits metastasis to lung in the tail-vein injection and the oral cavity xenograft models. Our findings highlight ROS1 as a candidate biomarker and therapeutic target for OSCC. Finally, we demonstrate that co-targeting of ROS1 and EGFR could potentially offer an effective oral cancer therapy.

MeSH terms

  • Animals
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Squamous Cell / drug therapy
  • Carcinoma, Squamous Cell / genetics*
  • Carcinoma, Squamous Cell / pathology*
  • Cell Line, Tumor
  • Cell Proliferation
  • Chemokine CXCL1 / metabolism
  • Down-Regulation
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • ErbB Receptors / antagonists & inhibitors
  • Gene Expression Regulation, Neoplastic*
  • Histones / metabolism
  • Humans
  • Lung Neoplasms / secondary*
  • Male
  • Methylation
  • Mice
  • Molecular Targeted Therapy / methods
  • Mouth Neoplasms / drug therapy
  • Mouth Neoplasms / genetics*
  • Mouth Neoplasms / pathology*
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / metabolism*
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / metabolism*
  • STAT1 Transcription Factor / metabolism
  • Up-Regulation
  • Xenograft Model Antitumor Assays
  • Zinc Finger Protein GLI1 / metabolism

Substances

  • Biomarkers, Tumor
  • CXCL1 protein, human
  • Chemokine CXCL1
  • GLI1 protein, human
  • Histones
  • Proto-Oncogene Proteins
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Zinc Finger Protein GLI1
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • EGFR protein, human
  • ErbB Receptors
  • Protein-Tyrosine Kinases
  • ROS1 protein, human