RNA binding protein RBM3 increases β-catenin signaling to increase stem cell characteristics in colorectal cancer cells

Mol Carcinog. 2016 Nov;55(11):1503-1516. doi: 10.1002/mc.22404. Epub 2015 Aug 31.

Abstract

Colorectal cancer (CRC) is the second leading cause of cancer deaths in the United States. It arises from loss of intestinal epithelial homeostasis and hyperproliferation of the crypt epithelium. In order to further understand the pathogenesis of CRC it is important to further understand the factors regulating intestinal epithelial proliferation and more specifically, regulation of the intestinal epithelial stem cell compartment. Here, we investigated the role of the RNA binding protein RBM3 in stem cell homeostasis in colorectal cancers. Using a doxycycline (Dox) inducible RBM3 overexpressing cell lines HCT 116 and DLD-1, we measured changes in side population (SP) cells that have high xenobiotic efflux capacity and increased capacity for self-renewal. In both cell lines, RBM3 induction showed significant increases in the percentage of side population cells. Additionally, we observed increases in spheroid formation and in cells expressing DCLK1, LGR5 and CD44Hi . As the Wnt/β-catenin signaling pathway is important for both physiologic and cancer stem cells, we next investigated the effects of RBM3 overexpression on β-catenin activity. RBM3 overexpression increased levels of nuclear β-catenin as well as TCF/LEF transcriptional activity. In addition, there was inactivation of GSK3β leading to decreased β-catenin phosphorylation. Pharmacologic inhibition of GSK3β using (2'Z,3'E)-6-Bromoindirubin-3'-oxime (BIO) also recapitulates the RBM3 induced β-catenin activity. In conclusion, we see that RNA binding protein RBM3 induces stemness in colorectal cancer cells through a mechanism involving suppression of GSK3β activity thereby enhancing β-catenin signaling. © 2015 Wiley Periodicals, Inc.

Keywords: CD44; DCLK1; GSK3β; LGR5; Wnt signaling; cancer stem cells.

MeSH terms

  • Cell Line, Tumor
  • Cell Proliferation
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology*
  • Doxycycline / pharmacology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glycogen Synthase Kinase 3 beta / metabolism
  • HCT116 Cells
  • Humans
  • Neoplastic Stem Cells / cytology*
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / metabolism
  • Phosphorylation
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism*
  • Wnt Proteins / metabolism
  • Wnt Signaling Pathway
  • beta Catenin / metabolism*

Substances

  • CTNNB1 protein, human
  • RBM3 protein, human
  • RNA-Binding Proteins
  • Wnt Proteins
  • beta Catenin
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Doxycycline