β-Catenin determines upper airway progenitor cell fate and preinvasive squamous lung cancer progression by modulating epithelial-mesenchymal transition

J Pathol. 2012 Mar;226(4):575-87. doi: 10.1002/path.3962. Epub 2012 Jan 17.

Abstract

Human lung cancers, including squamous cell carcinoma (SCC) are a leading cause of death and, whilst evidence suggests that basal stem cells drive SCC initiation and progression, the mechanisms regulating these processes remain unknown. In this study we show that β-catenin signalling regulates basal progenitor cell fate and subsequent SCC progression. In a cohort of preinvasive SCCs we established that elevated basal cell β-catenin signalling is positively associated with increased disease severity, epithelial proliferation and reduced intercellular adhesiveness. We demonstrate that transgene-mediated β-catenin inhibition within keratin 14-expressing basal cells delayed normal airway repair while basal cell-specific β-catenin activation increased cell proliferation, directed differentiation and promoted elements of early epithelial-mesenchymal transition (EMT), including increased Snail transcription and reduced E-cadherin expression. These observations are recapitulated in normal human bronchial epithelial cells in vitro following both pharmacological β-catenin activation and E-cadherin inhibition, and mirrored our findings in preinvasive SCCs. Overall, the data show that airway basal cell β-catenin determines cell fate and its mis-expression is associated with the development of human lung cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult Stem Cells / metabolism
  • Adult Stem Cells / pathology*
  • Animals
  • Biomarkers, Tumor / metabolism
  • Cadherins / genetics
  • Cadherins / metabolism
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology*
  • Cell Line, Transformed
  • Cell Lineage / physiology
  • Cell Proliferation
  • Cohort Studies
  • Disease Progression
  • Epithelial-Mesenchymal Transition*
  • Female
  • Humans
  • Keratin-14 / genetics
  • Keratin-14 / metabolism
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neoplasm Invasiveness
  • Signal Transduction
  • Snail Family Transcription Factors
  • Trachea / metabolism
  • Trachea / pathology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • beta Catenin / antagonists & inhibitors
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Biomarkers, Tumor
  • CTNNB1 protein, human
  • Cadherins
  • Keratin-14
  • Krt14 protein, mouse
  • Snail Family Transcription Factors
  • Transcription Factors
  • beta Catenin