Human papillomavirus-positivity is associated with EREG down-regulation and promoter hypermethylation in head and neck squamous cell carcinoma

Exp Mol Pathol. 2020 Dec:117:104549. doi: 10.1016/j.yexmp.2020.104549. Epub 2020 Sep 30.

Abstract

Background: Human papillomavirus (HPV) etiology has become evident in head and neck cancers (HNCs) and HPV positivity showed a strong association with its malignant progression. Since aberrant DNA methylation is known to drive carcinogenesis and progression in HNCs, we investigated to determine target gene(s) associated with this modification.

Methods: We characterized epigenetic changes in tumor-related genes (TRGs) that are known to be associated with HNC development and its progression.

Results: The expression levels of 42 candidate HNC-associated genes were analyzed. Of these, 7 TGRs (CHFR, RARβ, GRB7, EREG, RUNX2, RUNX3, and SMG-1) showed decreased expressions in HPV-positive (+) HNC cells compared with HPV-negative (-) HNC cells. When gene expression levels were compared corresponding to the DNA methylation conditions, GRB7 and EREG showed significant differential expression between HPV+ and HPV- cells, which suggested these genes as primary targets of epigenetic regulation in HPV-induced carcinogenesis. Furthermore, treatment with a demethylation agent, 5-aza-2'-deoxycytidine (5-aza-dc), caused restoration of EREG expression and was associated with hypomethylation of its promoter in HPV+ cells, while no changes was noted in HPV- cells. EREG promoter hypermethylation in HPV+ cells was confirmed using methylation-specific PCR (MS-PCR).

Conclusion: We conclude that EREG is the target of epigenetic regulation in HPV+ HNCs and its suppressed expression through promoter hypermethylation is associated with the development of HPV-associated HNCs.

Keywords: Epigenetic silencing; Epiregulin (EREG); Head and neck cancer; Human papillomavirus (HPV); Promoter methylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alphapapillomavirus / genetics*
  • Alphapapillomavirus / pathogenicity
  • Azacitidine
  • Carcinogenesis / genetics
  • Cell Line, Tumor
  • DNA (Cytosine-5-)-Methyltransferase 1 / genetics
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA Methylation / genetics
  • DNA Methyltransferase 3A
  • Decitabine
  • Disease Progression
  • Epigenesis, Genetic*
  • Epiregulin / genetics*
  • Gene Expression Regulation, Neoplastic / genetics
  • Humans
  • Neoplasm Proteins / genetics
  • Promoter Regions, Genetic / 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

  • DNMT3A protein, human
  • EREG protein, human
  • Epiregulin
  • Neoplasm Proteins
  • Decitabine
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNA (Cytosine-5-)-Methyltransferases
  • DNA Methyltransferase 3A
  • DNMT1 protein, human
  • Azacitidine