Post-translational glycoprotein modifications regulate colon cancer stem cells and colon adenoma progression in Apc(min/+) mice through altered Wnt receptor signaling

J Biol Chem. 2014 Nov 7;289(45):31534-49. doi: 10.1074/jbc.M114.602680. Epub 2014 Oct 1.

Abstract

Deletion of GnT-V (MGAT5), which synthesizes N-glycans with β(1,6)-branched glycans, reduced the compartment of cancer stem cells (CSC) in the her-2 mouse model of breast cancer, leading to delay of tumor onset. Because GnT-V levels are also commonly up-regulated in colon cancer, we investigated their regulation of colon CSC and adenoma development. Anchorage-independent cell growth and tumor formation induced by injection of colon tumor cells into NOD/SCID mice were positively associated with GnT-V levels, indicating regulation of proliferation and tumorigenicity. Using Apc(min/+) mice with different GnT-V backgrounds, knock-out of GnT-V had no significant effect on the number of adenoma/mouse, but adenoma size was significantly reduced and accompanied increased survival of Apc(min/+) mice with GnT-V deletion (p < 0.01), suggesting an inhibition in the progression of colon adenoma caused by deletion of GnT-V. Decreased expression levels of GnT-V down-regulated the population of colon (intestine) CSC, affecting their ability for self-renewal and tumorigenicity in NOD/SCID mice. Furthermore, altered nuclear translocation of β-catenin and expression of Wnt target genes were positively associated with expression levels of GnT-V, indicating the regulation of canonical Wnt/β-catenin signaling. By overexpressing the Wnt receptor, FZD-7, in colon cancer cells, we found that FZD-7 receptors expressed N-linked β(1,6) branching, indicating that FZD-7 can be modified by GnT-V. The aberrant Wnt signaling observed after modulating GnT-V levels is likely to result from altered N-linked β(1,6) branching on FZD-7, thereby affecting Wnt signaling, the compartment of CSC, and tumor progression.

Keywords: Apcmin/+ Mice; Cancer Stem Cells; Colon Cancer; Gene Knockout; GnT-V; N-Linked Glycosylation; Wnt Signaling.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Adenoma / metabolism*
  • Adenomatous Polyposis Coli Protein / genetics
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Colonic Neoplasms / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Genes, APC
  • Glycoside Hydrolases / metabolism
  • Glycosylation
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, SCID
  • Mice, Transgenic
  • N-Acetylglucosaminyltransferases / metabolism*
  • Neoplasm Transplantation
  • Neoplastic Stem Cells / cytology*
  • Phenotype
  • Protein Processing, Post-Translational*
  • Signal Transduction
  • Wnt Proteins / metabolism

Substances

  • Adenomatous Polyposis Coli Protein
  • Wnt Proteins
  • N-Acetylglucosaminyltransferases
  • alpha-1,6-mannosylglycoprotein beta 1,6-N-acetylglucosaminyltransferase
  • Glycoside Hydrolases