MicroRNA-155 deletion promotes tumorigenesis in the azoxymethane-dextran sulfate sodium model of colon cancer

Am J Physiol Gastrointest Liver Physiol. 2016 Mar 15;310(6):G347-58. doi: 10.1152/ajpgi.00326.2015. Epub 2016 Jan 7.

Abstract

Clinical studies have linked microRNA-155 (miR-155) expression in the tumor microenvironment to poor prognosis. However, whether miR-155 upregulation is predictive of a pro- or antitumorigenic response is unclear, as the limited preclinical data available remain controversial. We examined miR-155 expression in tumor tissue from colon cancer patients. Furthermore, we investigated the role of this microRNA in proliferation and apoptosis, inflammatory processes, immune cell populations, and transforming growth factor-β/SMAD signaling in a chemically induced (azoxymethane-dextran sulfate sodium) mouse model of colitis-associated colon cancer. We found a higher expression of miR-155 in the tumor region than in nontumor colon tissue of patients with colon cancer. Deletion of miR-155 in mice resulted in a greater number of polyps/adenomas, an increased symptom severity score, a higher grade of epithelial dysplasia, and a decrease in survival. Surprisingly, these findings were associated with an increase in apoptosis in the normal mucosa, but there was no change in proliferation. The protumorigenic effects of miR-155 deletion do not appear to be driven solely by dysregulation of inflammation, as both genotypes had relatively similar levels of inflammatory mediators. The enhanced tumorigenic response in miR-155(-/-) mice was associated with alterations in macrophages and neutrophils, as markers for these populations were decreased and increased, respectively. Furthermore, we demonstrated a greater activation of the transforming growth factor-β/SMAD pathway in miR-155(-/-) mice, which was correlated with the increased tumorigenesis. Given the multiple targets of miR-155, careful evaluation of its role in tumorigenesis is necessary prior to any consideration of its potential as a biomarker and/or therapeutic target in colon cancer.

Keywords: TGFβ/SMAD signaling pathway; colon cancer; immune cell markers; inflammation; miR-155.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Azoxymethane
  • Biomarkers
  • Carcinogens
  • Cell Proliferation
  • Colonic Neoplasms / chemically induced*
  • Colonic Neoplasms / genetics*
  • Colonic Neoplasms / pathology
  • Dextran Sulfate
  • Gene Deletion
  • Humans
  • Intestinal Mucosa / pathology
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics*
  • Signal Transduction / genetics
  • Smad Proteins / genetics
  • Transfection
  • Transforming Growth Factor beta / genetics

Substances

  • Biomarkers
  • Carcinogens
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • Smad Proteins
  • Transforming Growth Factor beta
  • Dextran Sulfate
  • Azoxymethane