The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development

Gastroenterology. 2009 Mar;136(3):967-77. doi: 10.1053/j.gastro.2008.12.003. Epub 2008 Dec 3.

Abstract

Background & aims: Gastric cancer is the second most common cause of cancer-related mortality worldwide, mainly as a result of late-stage detection. Interleukin (IL)-11 is a multifunctional cytokine reported to be up-regulated in human gastric cancer.

Methods: We investigated the importance of IL-11 in gastric cancer progression by examining its role in a variety of mouse gastric tumor models, as well as in nonneoplastic and tumor tissues taken from gastric cancer patients. We then determined the transcriptional and translational outcomes of IL-11 overexpression in normal gastric mucosa and identified a novel gene signature important early in the progression toward gastric tumorigenesis.

Results: IL-11 was up-regulated significantly in 4 diverse mouse models of gastric pathology as well as in human biopsy specimens adjacent to and within gastric cancer. Removal of IL-11 co-receptor alpha significantly reduced HKbeta-/- mouse fundic hyperplasia and ablated gp130(757F/F) mouse tumorigenesis. Exogenous IL-11 but not IL-6 activated oncogenic signal transducer and activator of transcription-3, and altered expression of novel proliferative and cytoprotective genes RegIII-beta, RegIII-gamma, gremlin-1, clusterin, and growth arrest specific-1 in wild-type gastric mucosa, a gene signature common in gp130(757F/F) and HKbeta-/- tumors as well as nonneoplastic mucosa of gastric cancer patients. One week of chronic IL-11 administration in wild-type mice sustained the gene signature, causing pretumorigenic changes in both antrum and fundus.

Conclusions: Increased gastric IL-11 alters expression of proliferative and cytoprotective genes and promotes pretumorigenic cellular changes.

MeSH terms

  • Animals
  • Biopsy
  • Cytokine Receptor gp130 / genetics
  • Cytokine Receptor gp130 / metabolism
  • Disease Models, Animal
  • Epithelial Cells / pathology
  • Epithelial Cells / physiology*
  • Gastric Fundus / pathology
  • Gastric Fundus / physiology
  • Gastric Mucosa / pathology
  • Gastric Mucosa / physiopathology
  • Gene Expression Regulation, Neoplastic
  • H(+)-K(+)-Exchanging ATPase / genetics
  • H(+)-K(+)-Exchanging ATPase / metabolism
  • Homeostasis / physiology
  • Humans
  • Hyperplasia
  • Interleukin-11 / genetics*
  • Interleukin-11 / metabolism*
  • Interleukin-11 / pharmacology
  • Interleukin-11 Receptor alpha Subunit / metabolism
  • Interleukin-6 / pharmacology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Oligonucleotide Array Sequence Analysis
  • Proto-Oncogene Proteins c-akt / metabolism
  • Pyloric Antrum / pathology
  • Pyloric Antrum / physiology
  • STAT3 Transcription Factor / metabolism
  • Stomach Neoplasms / pathology*
  • Stomach Neoplasms / physiopathology*

Substances

  • IL11 protein, human
  • Il11ra1 protein, mouse
  • Il6st protein, mouse
  • Interleukin-11
  • Interleukin-11 Receptor alpha Subunit
  • Interleukin-6
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Cytokine Receptor gp130
  • Proto-Oncogene Proteins c-akt
  • H(+)-K(+)-Exchanging ATPase