Expression and regulation of tumor necrosis factor alpha in normal and malignant ovarian epithelium

Mol Cancer Ther. 2006 Feb;5(2):382-90. doi: 10.1158/1535-7163.MCT-05-0303.

Abstract

Epidemiologic studies implicate inflammatory stimuli in the development of ovarian cancer. The proinflammatory cytokine tumor necrosis factor alpha (TNF-alpha) and both its receptors (TNFRI and TNFRII) are expressed in biopsies of this malignancy. Here, we tested the hypothesis that TNF-alpha is a regulator of the proinflammatory microenvironment of ovarian cancer. A cancer profiling array showed higher expression of TNF-alpha in ovarian tumors compared with normal ovarian tissue, and cultured ovarian cancer cells expressed up to 1,000 times more TNF-alpha mRNA than cultured normal ovarian surface epithelial cells; TNF-alpha protein was only detected in the supernatant of tumor cell cultures. Treatment with TNF-alpha induced TNF-alpha mRNA via TNFRI in both malignant and normal cells with evidence for enhanced TNF-alpha mRNA stability in tumor cells. TNF-alpha induced TNF-alpha protein in an autocrine fashion in tumor but not in normal ovarian surface epithelial cells. The TNF-alpha neutralizing antibody infliximab reduced the constitutive levels of TNF-alpha mRNA in tumor cell lines capable of autocrine TNF-alpha production. Apart from TNF-alpha mRNA expression, several other proinflammatory cytokines were constitutively expressed in malignant and normal ovarian surface epithelial cells, including interleukin (IL)-1alpha, IL-6, CCL2, CXCL8, and M-CSF. TNF-alpha treatment further induced these cytokines with de novo transcription of IL-6 mRNA contrasting with the increased stability of CCL2 mRNA. RNA interference directed against TNF-alpha was highly effective in abolishing constitutive IL-6 production by ovarian tumor cells. In summary, we show that TNF-alpha is differentially regulated in ovarian cancer cells compared with untransformed cells and modulates production of several cytokines that may promote ovarian tumorigenesis. Infliximab treatment may have a role in suppressing the TNF-alpha-driven inflammatory response associated with ovarian cancer.

Publication types

  • Comparative Study

MeSH terms

  • Antibodies, Monoclonal / pharmacology
  • Cell Line, Tumor
  • Chemokine CCL2 / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Epithelium / drug effects
  • Epithelium / metabolism
  • Female
  • Humans
  • Infliximab
  • Interleukin-6 / metabolism
  • Ovarian Neoplasms / genetics
  • Ovarian Neoplasms / metabolism*
  • Ovary / drug effects
  • Ovary / metabolism*
  • RNA Interference
  • RNA Stability
  • RNA, Messenger / analysis
  • RNA, Messenger / metabolism
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • Antibodies, Monoclonal
  • CCL2 protein, human
  • Chemokine CCL2
  • Cytokines
  • Interleukin-6
  • RNA, Messenger
  • Tumor Necrosis Factor-alpha
  • Infliximab