Reproductive hormone-induced, STAT3-mediated interleukin 6 action in normal and malignant human ovarian surface epithelial cells

J Natl Cancer Inst. 2002 Apr 17;94(8):617-29. doi: 10.1093/jnci/94.8.617.

Abstract

Background: Reproductive hormones are associated with risk for epithelial ovarian cancer. To determine the effect of such hormones on the activation of interleukin 6 (IL-6)/STAT3 (signal transducer and activator of transcription-3) signaling, which may be involved in ovarian cancer, we investigated the status of STAT3, IL-6, and its receptor in immortalized human ovarian surface epithelial (HOSE) and ovarian cancer (OVCA) cell lines.

Methods: Two immortalized HOSE cell lines and two OVCA cell lines were cultured with gonadotropins, sex steroid hormones, and/or IL-6, alone or with specific inhibitors or IL-6-neutralizing antibodies. Expression of IL-6, the IL-6 receptor alpha chain (IL-6Ralpha), and phosphorylated and unphosphorylated STAT3 messenger RNAs (mRNAs) and proteins in all cells was determined. Cell proliferation and soft-agar colony formation were assessed. STAT3 activity was investigated in OVCA cells transfected with a dominant negative STAT3 (Dn-STAT3), wild-type STAT3, or an empty control vector. All statistical tests were two-sided.

Results: Levels of IL-6 mRNA and protein increased in all cells treated with follicle-stimulating hormone (FSH), luteinizing hormone (LH), 17beta-estradiol, or estrone but increased only in OVCA cells treated with testosterone and 5alpha-dihydrotestosterone. For all lines, IL-6 antibodies partially inhibited hormone-stimulated cell proliferation but completely inhibited IL-6-enhanced cell proliferation. IL-6 induced STAT3 phosphorylation and activation in HOSE cells; STAT3 was constitutively activated in OVCA cells. Higher levels of IL-6Ralpha and STAT3 transcription factors were observed in OVCA cells than in HOSE cells. After transfection, Dn-STAT3 suppressed endogenous STAT3 and inhibited all forms of IL-6-stimulated OVCA cell proliferation (OVCA 429 cells, P<.001; OVCA 432 cells, P<.006), whereas wild-type STAT3 enhanced HOSE cell proliferation (wild-type STAT3 at 0.5 microg/mL in HOSE 306 cells, P<.002; STAT3 at 1.0 microg/mL in HOSE 306 or both concentrations of wild-type STAT3 in HOSE 642 cells, P<.001).

Conclusions: The IL-6/STAT3 signaling pathway may mediate FSH-, LH-, and estrogen-stimulated HOSE cell proliferation. Increased IL-6Ralpha expression and constitutive STAT3 activation may be associated with ovarian cancer.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adult
  • Antigens, CD / metabolism
  • Cell Division
  • Cell Line
  • Cytokine Receptor gp130
  • DNA-Binding Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Epithelial Cells / metabolism*
  • Female
  • Genes, Dominant
  • Gonadotropins / metabolism
  • Humans
  • Immunoblotting
  • Interleukin-6 / metabolism*
  • Membrane Glycoproteins / metabolism
  • Middle Aged
  • Ovarian Neoplasms / metabolism*
  • Ovary / metabolism*
  • RNA, Messenger / metabolism
  • Receptors, Interleukin-6 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • STAT3 Transcription Factor
  • Signal Transduction
  • Trans-Activators / metabolism*
  • Transfection
  • Tumor Cells, Cultured

Substances

  • Antigens, CD
  • DNA-Binding Proteins
  • Gonadotropins
  • IL6ST protein, human
  • Interleukin-6
  • Membrane Glycoproteins
  • RNA, Messenger
  • Receptors, Interleukin-6
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Trans-Activators
  • Cytokine Receptor gp130