A role for cancer-associated fibroblasts in inducing the epithelial-to-mesenchymal transition in human tongue squamous cell carcinoma

J Oral Pathol Med. 2014 Sep;43(8):585-92. doi: 10.1111/jop.12172. Epub 2014 Mar 20.

Abstract

Objectives: Lymph node metastasis is a prominent clinical feature of tongue squamous cell carcinoma (TSCC) and is associated with a higher mortality rate. Carcinoma-associated fibroblasts (CAFs), a major component of the tumor microenvironment (TME), play an important role in tumor progression, and are associated with a poor prognosis. The aim of this study was to examine the role of CAFs in promoting the invasion of TSCC through the epithelial-to-mesenchymal transition (EMT).

Materials and methods: A series of matched CAF and normal fibroblast (NF) pairs were assessed for cell morphology and for the expression of alpha smooth muscle actin (α-SMA), stromal cell-derived factor-1 (SDF1), fibroblast-activating protein (FAP), vimentin, and cytokeratin (CK) markers. Transwell assays, Western blot analysis, reverse transcription-PCR, and immunofluorescence staining were used to assess the role of CAFs, as compared to that of NFs, in promoting proliferation, migration, invasion, and EMT in TSCC.

Results: Both CAF and NF primary cultures expressed vimentin but not CK. CAFs showed significantly higher α-SMA protein levels, SDF1 secretion, and mRNA levels of α-SMA, SDF1, and FAP. We also found that co-culture with CAFs enhanced the proliferation and invasion of SCC9 cells. Moreover, co-culture with CAFs induced upregulation of the EMT markers fibronectin and vimentin, downregulation of E-cadherin, and enhanced invasion in SCC9 cells.

Conclusion: These results suggest that CAFs induce EMT marker expression and functional changes in TSCCs.

Keywords: cancer-associated fibroblasts; epithelial-mesenchymal transition; tongue squamous cancer cells; tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / analysis
  • Adult
  • Aged
  • Antigens, Neoplasm / analysis
  • Cadherins / analysis
  • Carcinoma, Squamous Cell / pathology*
  • Carcinoma, Squamous Cell / secondary
  • Cell Line, Tumor
  • Cell Movement / physiology
  • Cell Proliferation
  • Cell Shape
  • Cells, Cultured
  • Chemokine CXCL12 / analysis
  • Coculture Techniques
  • Endopeptidases
  • Epithelial-Mesenchymal Transition / physiology*
  • Female
  • Fibroblasts / pathology*
  • Fibroblasts / physiology
  • Fibronectins / analysis
  • Gelatinases / analysis
  • Humans
  • Keratins / analysis
  • Lymphatic Metastasis / pathology
  • Male
  • Membrane Proteins / analysis
  • Middle Aged
  • Neoplasm Invasiveness
  • Serine Endopeptidases / analysis
  • Tongue Neoplasms / pathology*
  • Tumor Microenvironment / physiology
  • Vimentin / analysis

Substances

  • ACTA2 protein, human
  • Actins
  • Antigens, Neoplasm
  • Cadherins
  • Chemokine CXCL12
  • Fibronectins
  • Membrane Proteins
  • Vimentin
  • Keratins
  • Endopeptidases
  • Serine Endopeptidases
  • fibroblast activation protein alpha
  • Gelatinases