Directional Migration in Esophageal Squamous Cell Carcinoma (ESCC) is Epigenetically Regulated by SET Nuclear Oncogene, a Member of the Inhibitor of Histone Acetyltransferase Complex

Neoplasia. 2017 Nov;19(11):868-884. doi: 10.1016/j.neo.2017.08.003. Epub 2017 Sep 19.

Abstract

Directional cell migration is of fundamental importance to a variety of biological events, including metastasis of malignant cells. Herein, we specifically investigated SET oncoprotein, a subunit of the recently identified inhibitor of acetyltransferases (INHAT) complex and identified its role in the establishment of front-rear cell polarity and directional migration in Esophageal Squamous Cell Carcinoma (ESCC). We further define the molecular circuits that govern these processes by showing that SET modulated DOCK7/RAC1 and cofilin signaling events. Moreover, a detailed analysis of the spatial distribution of RAC1 and cofilin allowed us to decipher the synergistical contributions of the two in coordinating the advancing dynamics by measuring architectures, polarities, and cytoskeletal organizations of the lamellipodia leading edges. In further investigations in vivo, we identified their unique role at multiple levels of the invasive cascade for SET cell and indicate the necessity for their functional balance to enable efficient invasion as well. Additionally, SET epigenetically repressed miR-30c expression by deacetylating histones H2B and H4 on its promoter, which was functionally important for the biological effects of SET in our cell-context. Finally, we corroborated our findings in vivo by evaluating the clinical relevance of SET signaling in the metastatic burden in mice and a large series of patients with ESCC at diagnosis, observing it's significance in predicting metastasis formation. Our findings uncovered a novel signaling network initiated by SET that epigenetically modulated ESCC properties and suggest that targeting the regulatory axis might be a promising strategy to inhibit migration and metastasis.

MeSH terms

  • Animals
  • Biomarkers, Tumor / biosynthesis
  • Biomarkers, Tumor / genetics
  • Carcinoma, Squamous Cell / genetics*
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Cell Movement / genetics*
  • DNA-Binding Proteins
  • Epigenesis, Genetic / genetics*
  • Esophageal Neoplasms / genetics*
  • Esophageal Neoplasms / metabolism
  • Esophageal Neoplasms / pathology
  • Esophageal Squamous Cell Carcinoma
  • GTPase-Activating Proteins / biosynthesis
  • GTPase-Activating Proteins / genetics
  • Guanine Nucleotide Exchange Factors
  • HEK293 Cells
  • Histone Acetyltransferases / biosynthesis
  • Histone Acetyltransferases / genetics*
  • Histone Chaperones / biosynthesis
  • Histone Chaperones / genetics*
  • Humans
  • Male
  • Mice
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Oncogenes / genetics*
  • Rats
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics*
  • rac1 GTP-Binding Protein / biosynthesis
  • rac1 GTP-Binding Protein / genetics

Substances

  • Biomarkers, Tumor
  • DNA-Binding Proteins
  • DOCK7 protein, human
  • GTPase-Activating Proteins
  • Guanine Nucleotide Exchange Factors
  • Histone Chaperones
  • Neoplasm Proteins
  • RAC1 protein, human
  • SET protein, human
  • Transcription Factors
  • Histone Acetyltransferases
  • rac1 GTP-Binding Protein