Synbindin in extracellular signal-regulated protein kinase spatial regulation and gastric cancer aggressiveness

J Natl Cancer Inst. 2013 Nov 20;105(22):1738-49. doi: 10.1093/jnci/djt271. Epub 2013 Oct 8.

Abstract

Background: The molecular mechanisms that control the aggressiveness of gastric cancer (GC) remain poorly defined. Here we show that synbindin contributes to the aggressiveness of GC by activating extracellular signal-regulated protein kinase (ERK) signaling on the Golgi apparatus.

Methods: Expression of synbindin was examined in normal gastric mucosa (n = 44), intestinal metaplastic gastric mucosa (n = 66), and GC tissues (n=52), and the biological effects of synbindin on tumor growth and ERK signaling were detected in cultured cells, nude mice, and human tissue samples. The interaction between synbindin and mitogen-activated protein kinase kinase (MEK1)/ERK was determined by immunofluorescence and fluorescence resonance energy transfer assays. The transactivation of synbindin by nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) was detected using luciferase reporter assay and chromatin immunoprecipitation.

Results: High expression of synbindin was associated with larger tumor size (120.8 vs 44.8 cm(3); P = .01), advanced tumor node metastasis (TNM) stage (P = .003), and shorter patient survival (hazard ratio = 1.51; 95% confidence interval [CI] = 1.01 to 2.27; P = .046). Synbindin promotes cell proliferation and invasion by activating ERK2 on the Golgi apparatus, and synbindin is directly transactivated by NF-κB. Synbindin expression level was statistically significantly higher in human GCs with activated ERK2 than those with low ERK2 activity (intensity score of 11.5, 95% CI = 10.4 to 12.4 vs intensity score of 4.6, 95% CI 3.9 to 5.3; P < .001). Targeting synbindin in xenograft tumors decreased ERK2 phosphorylation and statistically significantly reduced tumor volume (451.2mm(3), 95% CI = 328.3 to 574.1 vs 726.1mm(3), 95% CI = 544.2 to 908.2; P = .01).

Conclusions: Synbindin contributes to malignant phenotypes of GC by activating ERK on the Golgi, and synbindin is a potential biomarker and therapeutic target for GC.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chromatin Immunoprecipitation
  • Flow Cytometry
  • Fluorescence Resonance Energy Transfer
  • Fluorescent Antibody Technique
  • Gastric Mucosa / metabolism
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Neoplastic
  • Golgi Apparatus / enzymology
  • Golgi Apparatus / metabolism*
  • Heterografts
  • Humans
  • Kaplan-Meier Estimate
  • Luciferases
  • Luminescent Agents
  • MAP Kinase Kinase 1 / metabolism*
  • MAP Kinase Signaling System
  • Mice
  • Mice, Nude
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • NF-kappa B / metabolism*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Odds Ratio
  • Phosphorylation
  • Protein Array Analysis
  • Retrospective Studies
  • Stomach Neoplasms / enzymology
  • Stomach Neoplasms / metabolism*
  • Stomach Neoplasms / mortality
  • Stomach Neoplasms / pathology*
  • Transcriptional Activation
  • Up-Regulation
  • Vesicular Transport Proteins / genetics
  • Vesicular Transport Proteins / metabolism*

Substances

  • Luminescent Agents
  • NF-kappa B
  • Nerve Tissue Proteins
  • TRAPPC4 protein, human
  • Trappc4 protein, mouse
  • Vesicular Transport Proteins
  • Luciferases
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • MAP Kinase Kinase 1