Nicotine induces the up-regulation of the α7-nicotinic receptor (α7-nAChR) in human squamous cell lung cancer cells via the Sp1/GATA protein pathway

J Biol Chem. 2013 Nov 15;288(46):33049-59. doi: 10.1074/jbc.M113.501601. Epub 2013 Oct 2.

Abstract

Nicotine, the addictive component of cigarettes, promotes lung cancer proliferation via the α7-nicotinic acetylcholine receptor (α7-nAChR) subtype. The present manuscript explores the effect of nicotine exposure on α7-nAChR levels in squamous cell carcinoma of the lung (SCC-L) in vitro and in vivo. Nicotine (at concentrations present in the plasma of average smokers) increased α7-nAChR levels in human SCC-L cell lines. Nicotine-induced up-regulation of α7-nAChR was confirmed in vivo by chicken chorioallantoic membrane models. We also observed that the levels of α7-nAChR in human SCC-L tumors (isolated from patients who are active smokers) correlated with their smoking history. Nicotine increased the levels of α7-nAChR mRNA and α7-nAChR transcription in human SCC-L cell lines and SCC-L tumors. Nicotine-induced up-regulation of α7-nAChR required GATA4 and GATA6. ChIP assays showed that nicotine induced the binding of GATA4 or GATA6 to Sp1 on the α7-nAChR promoter, thereby inducing its transcription and increasing its levels in human SCC-L. Our data are clinically relevant because SCC-L patients smoked for decades before being diagnosed with cancer. It may be envisaged that continuous exposure to nicotine (in such SCC-L patients) causes up-regulation of α7-nAChRs, which facilitates tumor growth and progression. Our results will also be relevant to many SCC-L patients exposed to nicotine via second-hand smoke, electronic cigarettes, and patches or gums to quit smoking.

Keywords: GATA; Lung Cancer; Nicotinic Acetylcholine Receptors; Proliferation; Sp1.

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • Female
  • GATA4 Transcription Factor / genetics
  • GATA4 Transcription Factor / metabolism*
  • GATA6 Transcription Factor / genetics
  • GATA6 Transcription Factor / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Gene Expression Regulation, Neoplastic / genetics
  • Humans
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / pathology
  • Male
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • Neoplasms, Squamous Cell / genetics
  • Neoplasms, Squamous Cell / metabolism*
  • Neoplasms, Squamous Cell / pathology
  • Nicotine / pharmacology*
  • Nicotinic Agonists / pharmacology*
  • Response Elements
  • Smoking / adverse effects
  • Smoking / genetics
  • Smoking / metabolism
  • Smoking / pathology
  • Sp1 Transcription Factor / genetics
  • Sp1 Transcription Factor / metabolism*
  • Tobacco Smoke Pollution
  • Up-Regulation / drug effects
  • Up-Regulation / genetics
  • alpha7 Nicotinic Acetylcholine Receptor / biosynthesis*
  • alpha7 Nicotinic Acetylcholine Receptor / genetics

Substances

  • GATA4 Transcription Factor
  • GATA4 protein, human
  • GATA6 Transcription Factor
  • GATA6 protein, human
  • Neoplasm Proteins
  • Nicotinic Agonists
  • Sp1 Transcription Factor
  • Tobacco Smoke Pollution
  • alpha7 Nicotinic Acetylcholine Receptor
  • Nicotine