Grainyhead-like-2, an epithelial master programmer, promotes interferon induction and suppresses breast cancer recurrence

Mol Immunol. 2024 Jun:170:156-169. doi: 10.1016/j.molimm.2024.04.012. Epub 2024 Apr 30.

Abstract

Type-I and -III interferons play a central role in immune rejection of pathogens and tumors, thus promoting immunogenicity and suppressing tumor recurrence. Double strand RNA is an important ligand that stimulates tumor immunity via interferon responses. Differentiation of embryonic stem cells to pluripotent epithelial cells activates the interferon response during development, raising the question of whether epithelial vs. mesenchymal gene signatures in cancer potentially regulate the interferon pathway as well. Here, using genomics and signaling approaches, we show that Grainyhead-like-2 (GRHL2), a master programmer of epithelial cell identity, promotes type-I and -III interferon responses to double-strand RNA. GRHL2 enhanced the activation of IRF3 and relA/NF-kB and the expression of IRF1; a functional GRHL2 binding site in the IFNL1 promoter was also identified. Moreover, time to recurrence in breast cancer correlated positively with GRHL2 protein expression, indicating that GRHL2 is a tumor recurrence suppressor, consistent with its enhancement of interferon responses. These observations demonstrate that epithelial cell identity supports interferon responses in the context of cancer.

Keywords: Epithelial-mesenchymal transition; Grainyhead-like-2; IRF-3; Interferon; Tumor recurrence.

Publication types

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

MeSH terms

  • Animals
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / immunology
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Interferon Regulatory Factor-1 / genetics
  • Interferon Regulatory Factor-1 / immunology
  • Interferon Regulatory Factor-1 / metabolism
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / metabolism
  • Interferons / genetics
  • Interferons / immunology
  • Interferons / metabolism
  • Neoplasm Recurrence, Local / immunology
  • RNA, Double-Stranded / immunology
  • Signal Transduction / immunology
  • Transcription Factor RelA / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / immunology
  • Transcription Factors* / metabolism

Substances

  • DNA-Binding Proteins
  • GRHL2 protein, human
  • Interferon Regulatory Factor-1
  • Interferon Regulatory Factor-3
  • Interferons
  • IRF3 protein, human
  • RNA, Double-Stranded
  • Transcription Factor RelA
  • Transcription Factors