Differential regulation of gastric tumor growth by cytokines that signal exclusively through the coreceptor gp130

Gastroenterology. 2005 Sep;129(3):1005-18. doi: 10.1053/j.gastro.2005.06.068.

Abstract

Background & aims: We have shown that mice with a mutation in gp130 (gp130(757F/F)), the signal transducing receptor for interleukin (IL)-6 family cytokines, have chronic gastric inflammation and develop distal stomach tumors associated with deregulated phosphorylated STAT3 expression. This model recapitulates many characteristics of intestinal-type gastric cancer in humans.

Methods: To evaluate the role of IL-6 and IL-11 as ligands regulating tumor growth and submucosal invasion, we compared tumor characteristics of gp130(757F/F) mice with gp130(757F/F) mice lacking IL-6 or mature T and B cells.

Results: As a result of the gp130(757F/F) mutation, expression of IL-6 and IL-11 was greatly up-regulated concomitant with activation of STAT3 and development of tumors. However, the lack of IL-6 or T and B cells did not impact on tumor growth. While IL-6 did not regulate tumor growth or tumor vascularization, gp130(757F/F)/IL-6(-/-) mice showed approximately 10-20-fold more submucosal tumor invasion, reduced mononuclear inflammatory cell infiltrate, and greater IL-11 and matrix metalloproteinase (MMP)-13 and MMP-9 synthesis than gp130(757F/F) mice. Expression of MMP-13 was largely restricted to tumor-associated stroma, but MMP-9 was also expressed in polymorphonuclear cells and a subset of epithelial cells. In addition, treatment with recombinant IL-11 stimulated expression of MMP-13 and MMP-9 in stomachs of wild-type mice.

Conclusions: Increased submucosal invasion in gp130(757F/F)/IL-6(-/-) mice could not be explained by increased vascularization or reduced immunosurveillance but was most likely facilitated by augmented metalloproteinase activity driven by elevated IL-11 levels.

MeSH terms

  • Animals
  • Antigens, CD / drug effects
  • Antigens, CD / genetics
  • Antigens, CD / physiology*
  • Apoptosis
  • Base Sequence
  • Cytokine Receptor gp130
  • Cytokines / pharmacology*
  • DNA Primers
  • DNA-Binding Proteins / genetics
  • Gastric Mucosa / immunology
  • Gastric Mucosa / pathology
  • Gene Expression Regulation, Neoplastic / drug effects
  • In Situ Hybridization
  • Interleukin-11 / genetics
  • Interleukin-11 / pharmacology
  • Interleukin-6 / genetics
  • Interleukin-6 / pharmacology
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / drug effects
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutagenesis, Site-Directed
  • Polymerase Chain Reaction
  • STAT3 Transcription Factor
  • Signal Transduction / drug effects
  • Stomach Neoplasms / genetics
  • Stomach Neoplasms / pathology*
  • Trans-Activators / genetics

Substances

  • Antigens, CD
  • Cytokines
  • DNA Primers
  • DNA-Binding Proteins
  • Il6st protein, mouse
  • Interleukin-11
  • Interleukin-6
  • Membrane Glycoproteins
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Trans-Activators
  • Cytokine Receptor gp130