NeuroD1 mediates nicotine-induced migration and invasion via regulation of the nicotinic acetylcholine receptor subunits in a subset of neural and neuroendocrine carcinomas

Mol Biol Cell. 2014 Jun;25(11):1782-92. doi: 10.1091/mbc.E13-06-0316. Epub 2014 Apr 9.

Abstract

Cigarette smoking is a major risk factor for acquisition of small cell lung cancer (SCLC). A role has been demonstrated for the basic helix-loop-helix transcription factor NeuroD1 in the pathogenesis of neural and neuroendocrine lung cancer, including SCLC. In the present study we investigate the possible function of NeuroD1 in established tumors, as well as actions early on in pathogenesis, in response to nicotine. We demonstrate that nicotine up-regulates NeuroD1 in immortalized normal bronchial epithelial cells and a subset of undifferentiated carcinomas. Increased expression of NeuroD1 subsequently leads to regulation of expression and function of the nicotinic acetylcholine receptor subunit cluster of α3, α5, and β4. In addition, we find that coordinated expression of these subunits by NeuroD1 leads to enhanced nicotine-induced migration and invasion, likely through changes in intracellular calcium. These findings suggest that aspects of the pathogenesis of neural and neuroendocrine lung cancers may be affected by a nicotine- and NeuroD1-induced positive feedback loop.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Bronchi / pathology
  • Calcium / metabolism
  • Carcinoma, Neuroendocrine / metabolism*
  • Carcinoma, Neuroendocrine / pathology*
  • Cell Differentiation / drug effects
  • Cell Line, Tumor
  • Cell Movement / drug effects*
  • Clone Cells
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Lung Neoplasms / pathology
  • Models, Biological
  • Mutation
  • Neoplasm Invasiveness
  • Nerve Tissue Proteins / metabolism*
  • Nicotine / pharmacology*
  • Protein Subunits / metabolism*
  • Receptor, trkB / metabolism
  • Receptors, Nicotinic / metabolism*
  • Tumor Suppressor Protein p53 / metabolism
  • Up-Regulation / drug effects

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Nerve Tissue Proteins
  • Protein Subunits
  • Receptors, Nicotinic
  • Tumor Suppressor Protein p53
  • Neurogenic differentiation factor 1
  • Nicotine
  • Receptor, trkB
  • Extracellular Signal-Regulated MAP Kinases
  • Calcium