Hypoxia Induces Epithelial-Mesenchymal Transition in Follicular Thyroid Cancer: Involvement of Regulation of Twist by Hypoxia Inducible Factor-1α

Yonsei Med J. 2015 Nov;56(6):1503-14. doi: 10.3349/ymj.2015.56.6.1503.

Abstract

Purpose: Although follicular thyroid cancer (FTC) has a relatively fair prognosis, distant metastasis sometimes results in poor prognosis and survival. There is little understanding of the mechanisms contributing to the aggressiveness potential of thyroid cancer. We showed that hypoxia inducible factor-1α (HIF-1α) induced aggressiveness in FTC cells and identified the underlying mechanism of the HIF-1α-induced invasive characteristics.

Materials and methods: Cells were cultured under controlled hypoxic environments (1% O₂) or normoxic conditions. The effect of hypoxia on HIF-1α, and epithelial-to-mesenchymal transition (EMT) related markers were evaluated by quantitative real-time PCR, Western blot analysis and immunocytochemistry. Invasion and wound healing assay were conducted to identify functional character of EMT. The involvement of HIF-1α and Twist in EMT were studied using gene overexpression or silencing. After orthotopic nude mouse model was established using the cells transfected with lentiviral shHIF-1α, tissue analysis was done.

Results: Hypoxia induces HIF-1α expression and EMT, including typical morphologic changes, cadherin shift, and increased vimentin expression. We showed that overexpression of HIF-1α via transfection resulted in the aforementioned changes without hypoxia, and repression of HIF-1α with RNA interference suppressed hypoxia-induced HIF-1α and EMT. Furthermore, we also observed that Twist expression was regulated by HIF-1α. These were confirmed in the orthotopic FTC model.

Conclusion: Hypoxia induced HIF-1α, which in turn induced EMT, resulting in the increased capacity for invasion and migration of cells via regulation of the Twist signal pathway in FTC cells. These findings provide insight into a possible therapeutic strategy to prevent invasive and metastatic FTC.

Keywords: Hypoxia; Twist; epithelial-mesenchymal transition; follicular thyroid cancer; hypoxia inducible factor-1α; orthotopic thyroid cancer model.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma, Follicular / genetics*
  • Adenocarcinoma, Follicular / metabolism
  • Animals
  • Cadherins / genetics
  • Epithelial-Mesenchymal Transition / genetics*
  • Gene Expression Regulation, Neoplastic
  • Hypoxia / genetics*
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Lymphokines
  • Mice
  • Neoplasm Invasiveness
  • Phenotype
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Thyroid Neoplasms / genetics*
  • Thyroid Neoplasms / metabolism
  • Transcriptional Activation
  • Twist-Related Protein 1 / genetics*
  • Twist-Related Protein 1 / metabolism
  • Vimentin / metabolism

Substances

  • Cadherins
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Lymphokines
  • Twist-Related Protein 1
  • Vimentin
  • tumor migration inhibition factor

Supplementary concepts

  • Thyroid cancer, follicular