Targeting Epithelial-Mesenchymal Transition for Identification of Inhibitors for Pancreatic Cancer Cell Invasion and Tumor Spheres Formation

PLoS One. 2016 Oct 20;11(10):e0164811. doi: 10.1371/journal.pone.0164811. eCollection 2016.

Abstract

Background: Pancreatic cancer has an enrichment of stem-like cancer cells (CSCs) that contribute to chemoresistant tumors prone to metastasis and recurrence. Drug screening assays based on cytotoxicity cannot identify specific CSC inhibitors, because CSCs comprise only a small portion of cancer cell population, and it is difficult to propagate stable CSC populations in vitro for high-throughput screening (HTS) assays. Based on the important role of cancer cell epithelial-to-mesenchymal transition (EMT) in promoting CSCs, we hypothesized that inhibition of EMT can be a useful strategy for inhibiting CSCs, and therefore a feasible approach for HTS can be built for identification of CSC inhibitors, based on assays detecting EMT inhibition.

Methods: An immunofluorescent assay was established and optimized for HTS to identify compounds that enhance E-cadherin expression, as a hallmark of inhibition of EMT. Four chemical libraries containing 41,472 compounds were screened in PANC-1 pancreatic cancer cell line. Positive hits were validated for EMT and CSC inhibition in vitro using sphere formation assay, western blotting, immune fluorescence, and scratch assay.

Results: Initial hits were refined to 73 compounds with a secondary screening, among which 17 exhibited concentration dependent induction of E-cadherin expression. Six compounds were selected for further study which belonged to 2 different chemical structural clusters. A novel compound 1-(benzylsulfonyl) indoline (BSI, Compound #38) significantly inhibited pancreatic cancer cell migration and invasion. BSI inhibited histone deacetylase, increased histone 4 acetylation preferably, resulting in E-cadherin up-regulation. BSI effectively inhibited tumor spheres formation. Six more analogues of BSI were tested for anti-migration and anti-CSC activities.

Conclusion: This study demonstrated a feasible approach for discovery of agents targeting EMT and CSCs using HTS, and identified a class of novel chemicals that could be developed as anti-EMT and anti-CSC drug leads.

MeSH terms

  • CD24 Antigen / metabolism
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Epithelial Cell Adhesion Molecule / metabolism
  • Epithelial-Mesenchymal Transition / drug effects*
  • High-Throughput Screening Assays
  • Humans
  • Hyaluronan Receptors / metabolism
  • Microscopy, Fluorescence
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Small Molecule Libraries / chemistry
  • Small Molecule Libraries / toxicity*
  • Snail Family Transcription Factors / antagonists & inhibitors
  • Snail Family Transcription Factors / metabolism
  • Zonula Occludens-1 Protein / genetics
  • Zonula Occludens-1 Protein / metabolism

Substances

  • CD24 Antigen
  • Cadherins
  • EPCAM protein, human
  • Epithelial Cell Adhesion Molecule
  • Hyaluronan Receptors
  • Small Molecule Libraries
  • Snail Family Transcription Factors
  • TJP1 protein, human
  • Zonula Occludens-1 Protein