The IL-18 antagonist IL-18-binding protein is produced in the human ovarian cancer microenvironment

Clin Cancer Res. 2013 Sep 1;19(17):4611-20. doi: 10.1158/1078-0432.CCR-13-0568. Epub 2013 Jul 19.

Abstract

Purpose: Interleukin (IL)-18 is an immune-enhancing cytokine, which induces IFN-γ production, T-helper 1 responses, and antitumor effects. In turn, IFN-γ stimulates IL-18-binding protein production, which blocks IL-18 activity. In view of the potential use of IL-18 in epithelial ovarian cancer (EOC) immunotherapy, here, we studied IL-18BP expression and its regulation by cytokines in EOC cells in vitro and in vivo.

Experimental design: Expression and production of IL-18BP in EOC cell lines, primary ovarian carcinomas, and the corresponding normal tissues, patients' serum, and ascites were investigated by immunochemistry, ELISA, screening of gene expression profiles, and reverse-transcription PCR.

Results: Analysis of gene expression profiles revealed that IL18BP mRNA is increased in EOC tumors compared with normal ovary cells. Release of IL-18BP was detectable in EOC sera and to a greater extent in the ascites, indicating production at the tumor site. Indeed, immunochemical analyses on cells isolated from the ascites and on tumor sections indicated that IL-18BP is expressed in both tumor cells and tumor-associated leukocytes, which displayed a CD3-CD20-NKp46-CD13+CD14low phenotype. EOC cell lines do not constitutively express IL-18BP. However, its release is inducible both by IFN-γ stimulation in vitro and by xenotransplantation of EOC cells in immune-deficient mice, suggesting a role for the microenvironment. In vitro experiments and immunochemistry indicated that IL-27 is also involved in IL-18BP upregulation in EOC cell lines and primary cells through STAT1 activation. Together, these data indicate that IL-18BP, which is produced in EOC in response to microenvironmental factors, may inhibit endogenous or exogenous IL-18 activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunotherapy
  • Intercellular Signaling Peptides and Proteins / biosynthesis
  • Intercellular Signaling Peptides and Proteins / blood
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Interferon-gamma / genetics
  • Interleukin-18 / genetics
  • Interleukin-18 / metabolism*
  • Interleukins / metabolism
  • Mice
  • Middle Aged
  • Ovarian Neoplasms / blood*
  • Ovarian Neoplasms / genetics*
  • Ovarian Neoplasms / pathology
  • STAT1 Transcription Factor / metabolism
  • Tumor Microenvironment / genetics
  • Xenograft Model Antitumor Assays

Substances

  • Intercellular Signaling Peptides and Proteins
  • Interleukin-18
  • Interleukins
  • MYDGF protein, human
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • interleukin-18 binding protein
  • Interferon-gamma