Nicotine promotes proliferation of human nasopharyngeal carcinoma cells by regulating α7AChR, ERK, HIF-1α and VEGF/PEDF signaling

PLoS One. 2012;7(8):e43898. doi: 10.1371/journal.pone.0043898. Epub 2012 Aug 31.

Abstract

Nicotine, the major component in cigarette smoke, can promote tumor growth and angiogenesis, but the precise mechanisms involved remain largely unknown. Here, we investigated the mechanism of action of nicotine in human nasopharyngeal carcinoma (NPC) cells. Nicotine significantly promoted cell proliferation in a dose and time-dependent manner in human NPC cells. The mechanism studies showed that the observed stimulation of proliferation was accompanied by the nicotine-mediated simultaneous modulation of α7AChR, HIF-1α, ERK and VEGF/PEDF signaling. Treatment of NPC cells with nicotine markedly upregulated the expression of α7AChR and HIF-1α proteins. Transfection with a α7AChR or HIF-1α-specific siRNA or a α7AChR-selective inhibitor significantly attenuated the nicotine-mediated promotion of NPC cell proliferation. Nicotine also promoted the phosphorylation of ERK1/2 but not JNK and p38 proteins, thereby induced the activation of ERK/MAPK signaling pathway. Pretreatment with an ERK-selective inhibitor effectively reduced the nicotine-induced proliferation of NPC cells. Moreover, nicotine upregulated the expression of VEGF but suppressed the expression of PEDF at mRNA and protein levels, leading to a significant increase of the ratio of VEGF/PEDF in NPC cells. Pretreatment with a α7AChR or ERK-selective inhibitor or transfection with a HIF-1α-specific siRNA in NPC cells significantly inhibited the nicotine-induced HIF-1α expression and VEGF/PEDF ratio. These results therefore indicate that nicotine promotes proliferation of human NPC cells in vitro through simultaneous modulation of α7AChR, HIF-1α, ERK and VEGF/PEDF signaling and suggest that the related molecules such as HIF-1α might be the potential therapeutic targets for tobacco-associated diseases such as nasopharyngeal carcinomas.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinoma
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Dose-Response Relationship, Drug
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Eye Proteins / genetics
  • Eye Proteins / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Nasopharyngeal Carcinoma
  • Nasopharyngeal Neoplasms / pathology*
  • Nerve Growth Factors / genetics
  • Nerve Growth Factors / metabolism
  • Nicotiana / toxicity
  • Nicotine / pharmacology*
  • Receptors, Nicotinic / metabolism
  • Serpins / genetics
  • Serpins / metabolism
  • Signal Transduction / drug effects*
  • Time Factors
  • Up-Regulation / drug effects
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism
  • alpha7 Nicotinic Acetylcholine Receptor

Substances

  • Chrna7 protein, human
  • Eye Proteins
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Nerve Growth Factors
  • Receptors, Nicotinic
  • Serpins
  • Vascular Endothelial Growth Factor A
  • alpha7 Nicotinic Acetylcholine Receptor
  • pigment epithelium-derived factor
  • Nicotine
  • Extracellular Signal-Regulated MAP Kinases

Grants and funding

This work was supported from the National Natural Science Foundation of China (No. 81071687), the Ph.D. Programs Foundation of Ministry of Education of China, the State Key Laboratory of Oncology in Southern China, and the “985 Program” of Sun Yat-Sen University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.