miRomics and Proteomics Reveal a miR-296-3p/PRKCA/FAK/Ras/c-Myc Feedback Loop Modulated by HDGF/DDX5/β-catenin Complex in Lung Adenocarcinoma

Clin Cancer Res. 2017 Oct 15;23(20):6336-6350. doi: 10.1158/1078-0432.CCR-16-2813. Epub 2017 Jul 27.

Abstract

Purpose: This study was performed to identify the detailed mechanisms by which miR-296-3p functions as a tumor suppressor to prevent lung adenocarcinoma (LADC) cell growth, metastasis, and chemoresistance.Experimental Design: The miR-296-3p expression was examined by real-time PCR and in situ hybridization. MTT, EdU incorporation, Transwell assays, and MTT cytotoxicity were respectively performed for cell proliferation, metastasis, and chemoresistance; Western blotting was performed to analyze the pathways by miR-296-3p and HDGF/DDX5 complex. The miRNA microarray and luciferase reporter assays were respectively used for the HDGF-mediated miRNAs and target genes of miR-296-3p. The ChIP, EMSA assays, and coimmunoprecipitation combined with mass spectrometry and GST pull-down were respectively designed to analyze the DNA-protein complex and HDGF/DDX5/β-catenin complex.Results: We observed that miR-296-3p not only controls cell proliferation and metastasis, but also sensitizes LADC cells to cisplatin (DDP) in vitro and in vivo Mechanistic studies demonstrated that miR-296-3p directly targets PRKCA to suppress FAK-Ras-c-Myc signaling, thus stimulating its own expression in a feedback loop that blocks cell cycle and epithelial-mesenchymal transition (EMT) signal. Furthermore, we observed that suppression of HDGF-β-catenin-c-Myc signaling activates miR-296-3p, ultimately inhibiting the PRKCA-FAK-Ras pathway. Finally, we found that DDX5 directly interacts with HDGF and induces β-catenin-c-Myc, which suppresses miR-296-3p and further activates PRKCA-FAK-Ras, cell cycle, and EMT signaling. In clinical samples, reduced miR-296-3p is an unfavorable factor that inversely correlates with HDGF/DDX5, but not PRKCA.Conclusions: Our study provides a novel mechanism that the miR-296-3p-PRKCA-FAK-Ras-c-Myc feedback loop modulated by HDGF/DDX5/β-catenin complex attenuates cell growth, metastasis, and chemoresistance in LADC. Clin Cancer Res; 23(20); 6336-50. ©2017 AACR.

MeSH terms

  • Adenocarcinoma / genetics*
  • Adenocarcinoma / metabolism*
  • Adenocarcinoma / pathology
  • Adenocarcinoma of Lung
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • DEAD-box RNA Helicases / metabolism
  • Disease Models, Animal
  • Drug Resistance, Neoplasm / genetics
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Heterografts
  • Humans
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / pathology
  • Mice
  • MicroRNAs / genetics*
  • Multiprotein Complexes
  • Neoplasm Metastasis
  • Promoter Regions, Genetic
  • Protein Binding
  • Protein Kinase C-alpha / genetics
  • Protein Kinase C-alpha / metabolism
  • Proteome*
  • Proteomics
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • RNA Interference
  • Transcriptome*
  • beta Catenin / metabolism
  • ras Proteins / genetics
  • ras Proteins / metabolism

Substances

  • MIRN296 microRNA, human
  • MicroRNAs
  • Multiprotein Complexes
  • Proteome
  • Proto-Oncogene Proteins c-myc
  • beta Catenin
  • Focal Adhesion Kinase 1
  • PTK2 protein, human
  • PRKCA protein, human
  • Protein Kinase C-alpha
  • Ddx5 protein, human
  • DEAD-box RNA Helicases
  • ras Proteins