Epithelial to mesenchymal transition markers are associated with an increased metastatic risk in primary cutaneous squamous cell carcinomas but are attenuated in lymph node metastases

J Dermatol Sci. 2013 Nov;72(2):93-102. doi: 10.1016/j.jdermsci.2013.07.001. Epub 2013 Jul 15.

Abstract

Background: Cutaneous squamous cell carcinoma (cSCC) is the second most common malignancy in humans and approximately 5% metastasize, usually to regional lymph nodes. Epithelial to mesenchymal transition (EMT) is a process involving loss of intercellular adhesion, acquisition of a mesenchymal phenotype and enhanced migratory potential; epithelial markers, such as E-cadherin, are down-regulated and mesenchymal proteins (Vimentin), increased.

Objective: To investigate the expression of EMT markers in metastatic SCC (MSCC) and their corresponding metastases, and to correlate them with clinico-pathological factors associated with an increased risk of metastasis.

Methods: We performed a retrospective study that included 146 cSCC samples (51 primary non-metastatic, 56 primary metastatic, 39 lymphatic metastases). Immunohistochemistry for E-cadherin, Vimentin, Snail, beta-catenin, Twist, Zeb1 and Podoplanin was performed.

Results: Loss of membranous E-cadherin was observed in 77% cSCCs, with no differences between MSCC and non-MSCC. Among the transcriptional factors controlling EMT, no significant Snail1 expression was detected. Twist, Zeb1, Vimentin, beta-catenin and Podoplanin were significantly overexpressed in MSCCs. Twist ectopic expression in SCC13 cells induced Zeb1, Vimentin and Podoplanin expression and E-cadherin delocalization. These changes resulted in a scattered migration pattern in vitro. Expression of EMT markers was decreased in the metastases when compared with the corresponding primary tumors.

Conclusion: These results suggest that a partial EMT, characterized by the expression of Twist but without a total E-cadherin depletion, is involved in the acquisition of invasive traits by cSCC, but the process is downregulated in lymph node metastases.

Keywords: Cutaneous squamous cell carcinoma; E-cadherin; Epithelial to mesenchymal transition; Metastasis; Twist; Vimentin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD
  • Biomarkers, Tumor / metabolism*
  • Cadherins / metabolism
  • Carcinoma, Squamous Cell / metabolism*
  • Down-Regulation
  • Epithelial-Mesenchymal Transition*
  • Gene Expression Regulation, Neoplastic*
  • Homeodomain Proteins / metabolism
  • Humans
  • Immunohistochemistry
  • Lymphatic Metastasis*
  • Membrane Glycoproteins / metabolism
  • Nuclear Proteins / metabolism
  • Phenotype
  • Retrospective Studies
  • Risk
  • Skin Neoplasms / metabolism*
  • Snail Family Transcription Factors
  • Transcription Factors / metabolism
  • Twist-Related Protein 1 / metabolism
  • Vimentin / metabolism
  • Zinc Finger E-box-Binding Homeobox 1
  • beta Catenin / metabolism

Substances

  • Antigens, CD
  • Biomarkers, Tumor
  • CDH1 protein, human
  • CTNNB1 protein, human
  • Cadherins
  • Homeodomain Proteins
  • Membrane Glycoproteins
  • Nuclear Proteins
  • PDPN protein, human
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • TWIST1 protein, human
  • Transcription Factors
  • Twist-Related Protein 1
  • Vimentin
  • ZEB1 protein, human
  • Zinc Finger E-box-Binding Homeobox 1
  • beta Catenin