The PI3K/AKT/c-MYC Axis Promotes the Acquisition of Cancer Stem-Like Features in Esophageal Squamous Cell Carcinoma

Stem Cells. 2016 Aug;34(8):2040-51. doi: 10.1002/stem.2395. Epub 2016 May 23.

Abstract

The importance of intratumoral heterogeneity has been highlighted by the identification and characterization of cancer stem cells (CSCs). Based on the differential responsiveness to a Sox2 reporter, SRR2, we had found a novel dichotomy in esophageal squamous cell carcinoma (ESCC) cells, with reporter-responsive (RR) cells showing more CSC-like features than reporter-unresponsive (RU) cells. Specifically, RR cells exhibited significantly higher tumorsphere formation capacity, proportions of CD44(High) cells, chemoresistance to cisplatin, and tumorigenic potential in vivo. H2 O2 , a potent inducer of oxidative stress and reactive oxygen species, was found to induce a conversion from RU to RR cells; importantly, converted RR cells acquired CSC-like features. The PI3K/AKT/c-MYC signalling axis is important in this context, since pharmacologic blockade of PI3K-AKT or siRNA knockdown of c-MYC effectively inhibited the RR phenotype and its associated CSC-like features, as well as the H2 O2 -induced RU/RR conversion. In a cohort of 188 ESCC patient samples, we found a significant correlation between strong c-MYC expression and a short overall survival (p = .009). In conclusion, we have described a novel intratumoral heterogeneity in ESCC. The identification of the PI3K/AKT/c-MYC axis as a driver of CSC-like features carries therapeutic implications. Stem Cells 2016;34:2040-2051.

Keywords: Cancer stemness; Esophageal squamous cell carcinoma; Intra-tumoral heterogeneity; Oxidative stress; c-MYC.

MeSH terms

  • Carcinoma, Squamous Cell / metabolism*
  • Carcinoma, Squamous Cell / pathology*
  • Cell Line, Tumor
  • Esophageal Neoplasms / metabolism*
  • Esophageal Neoplasms / pathology*
  • Esophageal Squamous Cell Carcinoma
  • Female
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Male
  • Middle Aged
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • Oxidative Stress / drug effects
  • Phenotype
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Prognosis
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Proto-Oncogene Proteins c-myc / metabolism*
  • SOXB1 Transcription Factors / metabolism
  • Signal Transduction* / drug effects
  • Survival Analysis

Substances

  • Proto-Oncogene Proteins c-myc
  • SOXB1 Transcription Factors
  • Hydrogen Peroxide
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt