N-glycosylation induces the CTHRC1 protein and drives oral cancer cell migration

J Biol Chem. 2013 Jul 12;288(28):20217-27. doi: 10.1074/jbc.M113.473785. Epub 2013 May 23.

Abstract

Oral squamous cell carcinoma (OSCC) is one of the most pernicious malignancies, but the mechanisms underlying its development and progression are poorly understood. One of the key pathways implicated in OSCC is the canonical Wnt/β-catenin signaling pathway. Previously, we reported that canonical Wnt signaling functions in a positive feedback loop with the DPAGT1 gene, a principal regulator of the metabolic pathway of protein N-glycosylation, to hyperglycosylate E-cadherin and reduce intercellular adhesion. Here, we show that in OSCC, DPAGT1 and canonical Wnt signaling converge to up-regulate CTHRC1 (collagen triple helix repeat containing 1), an N-glycoprotein implicated in tumor invasion and metastasis. We found that in human OSCC specimens, amplification of the levels of CTHRC1 was associated with its hyperglycosylation. Partial inhibition of DPAGT1 expression in OSCC CAL27 cells reduced CTHRC1 abundance by increasing protein turnover, indicating that N-glycosylation stabilizes CTHRC1. Additionally, canonical Wnt signaling promoted β-catenin/T-cell factor transcriptional activity at the CTHRC1 promoter to further elevate CTHRC1 levels. We demonstrate that DPAGT1 promotes cell migration and drives the localization of CTHRC1 to cells at the leading edge of a wound front coincident with drastic changes in cell morphology. We propose that in OSCC, dysregulation of canonical Wnt signaling and DPAGT1-dependent N-glycosylation induces CTHRC1, thereby driving OSCC cell migration and tumor spread.

Keywords: CTHRC1; Cancer; Canonical Wnt; Cell Migration; DPAGT1; Glycoprotein; Glycosylation; OSCC; Wnt Signaling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism*
  • Carcinoma, Squamous Cell / pathology
  • Cell Line, Tumor
  • Cell Movement*
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism*
  • Gene Expression Regulation, Neoplastic
  • Glycosylation
  • Humans
  • Immunoblotting
  • Microscopy, Confocal
  • Mouth Neoplasms / genetics
  • Mouth Neoplasms / metabolism*
  • Mouth Neoplasms / pathology
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • TCF Transcription Factors / metabolism
  • Transferases (Other Substituted Phosphate Groups) / genetics
  • Transferases (Other Substituted Phosphate Groups) / metabolism
  • Wnt Proteins / metabolism
  • beta Catenin / metabolism

Substances

  • CTHRC1 protein, human
  • Extracellular Matrix Proteins
  • TCF Transcription Factors
  • Wnt Proteins
  • beta Catenin
  • Transferases (Other Substituted Phosphate Groups)
  • UDPacetylglucosamine-dolichyl-phosphate acetylglucosamine-1-phosphate transferase