Cyclooxygenase-2-dependent activation of signal transducer and activator of transcription 3 by interleukin-6 in non-small cell lung cancer

Clin Cancer Res. 2005 Nov 1;11(21):7674-82. doi: 10.1158/1078-0432.CCR-05-1205.

Abstract

Purpose: Cyclooxygenase-2 (COX-2), phosphorylated signal transducers and activators of transcription 3 (STAT3), and interleukin-6 (IL-6) are elevated in non-small cell lung cancer (NSCLC). These molecules affect numerous cellular pathways, including angiogenesis and apoptosis resistance, and, therefore, may act in concert in NSCLC.

Experimental design: We examined IL-6 and phosphorylated STAT3 in COX-2-overexpressing [COX-2 sense-oriented (COX-2-S)] NSCLC cells and control cells. The effect of IL-6, STAT3, phosphatidylinositol 3-kinase, and mitogen-activated protein/extracellular signal-regulated kinase kinase on vascular endothelial growth factor (VEGF) production and apoptosis resistance was assessed in COX-2-overexpresing cells.

Results: We report that NSCLC cells overexpressing COX-2 (COX-2-S) have increased IL-6 and phosphorylated STAT3 expression compared with control cells. IL-6 induced expression of VEGF in NSCLC cells. Moreover, blocking IL-6, mitogen-activated protein/extracellular signal-regulated kinase kinase, or phosphatidylinositol 3-kinase decreased VEGF production in COX-2-S cells. The addition of IL-6 to NSCLC cells resulted in increased apoptosis resistance. Furthermore, the inhibition of STAT3 or IL-6 induced apoptosis and reduced survivin expression, a member of the inhibitor of apoptosis protein family in COX-2-S cells.

Conclusions: Overall, these findings suggest a novel pathway in which COX-2 activates STAT3 by inducing IL-6 expression. This pathway could contribute to tumor formation by promoting survivin-dependent apoptosis resistance and VEGF production. These findings provide a rationale for the future development of STAT3, IL-6, and/or COX-2-targeted therapies for the treatment of lung cancer.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Apoptosis
  • Blotting, Western
  • Carcinoma, Non-Small-Cell Lung / metabolism*
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Survival
  • Cyclooxygenase 2 / biosynthesis*
  • Cyclooxygenase 2 / physiology*
  • Cytokines / metabolism
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Interleukin-6 / metabolism*
  • Lung Neoplasms / metabolism*
  • Neovascularization, Pathologic
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation
  • RNA / metabolism
  • RNA, Small Interfering / metabolism
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Cytokines
  • Enzyme Inhibitors
  • Interleukin-6
  • RNA, Small Interfering
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Vascular Endothelial Growth Factor A
  • RNA
  • Cyclooxygenase 2
  • Phosphatidylinositol 3-Kinases