Krüppel-like factor 4 is a novel prognostic predictor for urothelial carcinoma of bladder and it regulates TWIST1-mediated epithelial-mesenchymal transition

Urol Oncol. 2016 Nov;34(11):485.e15-485.e24. doi: 10.1016/j.urolonc.2016.07.002. Epub 2016 Aug 9.

Abstract

Background: Krüppel-like factor 4 (KLF4) exerts tumor suppressive or oncogenic functions in a cell-type-dependent manner, but its prognostic role in urothelial carcinoma of bladder (UCB) remains unclear. We aimed to determine how KLF4 regulates epithelial-mesenchymal transition (EMT) and predicts patient survival in UCB.

Patients and methods: The roles of KLF4 and other EMT regulators in cancer progression were studied in UCB specimens of 398 patients, UCB cell lines. The results were validated by open-access The Cancer Genome Atlas dataset.

Results: Over a median follow-up of 46.5 months, tissue microarray demonstrated that strong KLF4 expression was associated with higher risk toward metastasis and death (P<0.001). KLF4 expression positively correlated with TWIST1 and vimentin, and inversely correlated with E-cadherin expression. Metastasis-free survival was poorest in KLF4/TWIST1 coexpression group, followed by KLF4 or TWIST1 expression-alone group, and no-expression group (P<0.001). Multivariate analysis substantiated that KLF4/TWIST1 coexpression independently predicted overall mortality and metastasis risk with hazard ratios of 2.43 (95% CI: 1.65-3.64) and 7.54 (CI: 4.03-12.10). The Cancer Genome Atlas dataset of bladder cancer also revealed a trend toward decreased overall survival in the high KLF4 expression group as compared to the low KLF4 group. In vitro, KLF4 is accompanied with decreased E-cadherin and β-catenin expressions, increased vimentin and fibronectin expressions, and enhanced migration/invasion. KLF4 knockdown suppressed TWIST1 expression and inhibited EMT, migration and invasion, whereas enforced KLF4 overexpression activated TWIST1 expression and restored EMT and metastatic phenotype. Furthermore, TWIST1 knockdown abolished KLF4-faciliated EMT and metastatic feature without affecting KLF4 expression.

Conclusions: KLF4 promotes TWIST1-mediated EMT and may represent a novel prognostic predictor in UCB.

Keywords: Epithelial-mesenchymal transition; Krüppel-like factor 4; TWIST1; Urothelial carcinoma of bladder.

MeSH terms

  • Aged
  • Aged, 80 and over
  • Antigens, CD
  • Biomarkers, Tumor / analysis*
  • Cadherins / biosynthesis
  • Carcinoma, Transitional Cell / chemistry
  • Carcinoma, Transitional Cell / mortality
  • Carcinoma, Transitional Cell / pathology*
  • Cell Movement
  • Epithelial-Mesenchymal Transition / physiology*
  • Female
  • Fibronectins / biosynthesis
  • Follow-Up Studies
  • Humans
  • Kaplan-Meier Estimate
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / analysis
  • Kruppel-Like Transcription Factors / physiology*
  • Male
  • Middle Aged
  • Neoplasm Invasiveness
  • Neoplasm Metastasis
  • Neoplasm Proteins / analysis
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / physiology*
  • Nuclear Proteins / physiology*
  • Prognosis
  • Tissue Array Analysis
  • Tumor Cells, Cultured
  • Twist-Related Protein 1 / physiology*
  • Urinary Bladder Neoplasms / chemistry
  • Urinary Bladder Neoplasms / mortality
  • Urinary Bladder Neoplasms / pathology*
  • Vimentin / biosynthesis
  • beta Catenin / biosynthesis

Substances

  • Antigens, CD
  • Biomarkers, Tumor
  • CDH1 protein, human
  • CTNNB1 protein, human
  • Cadherins
  • Fibronectins
  • KLF4 protein, human
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • Neoplasm Proteins
  • Nuclear Proteins
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • Vimentin
  • beta Catenin