DC-SIGN-LEF1/TCF1-miR-185 feedback loop promotes colorectal cancer invasion and metastasis

Cell Death Differ. 2020 Jan;27(1):379-395. doi: 10.1038/s41418-019-0361-2. Epub 2019 Jun 19.

Abstract

DC-SIGN is previously focused on its physiologic and pathophysiologic roles in immune cells. Little is known about whether DC-SIGN is expressed in malignant epithelial cells and how DC-SIGN participates in tumor progression. Here we showed that DC-SIGN expression was increased in metastatic colorectal cancer (CRC) cell lines and patient tissues. The overall survival in CRC patients with positive DC-SIGN was remarkably reduced. Gain of DC-SIGN function facilitated the CRC metastases both in vitro and in vivo, and this effect was reversed by miR-185. DC-SIGN and Lyn interacted physically, and Lyn maintained the stability of DC-SIGN in cells. DC-SIGN activation recruited Lyn and p85 to form the DC-SIGN-Lyn-p85 complex, which promoted CRC metastasis by increasing PI3K/Akt/β-catenin signaling in tyrosine kinase Lyn-dependent manner. Furthermore, activation of DC-SIGN promoted the transcription of MMP-9 and VEGF by increasing PI3K/Akt/β-catenin signaling, and induced TCF1/LEF1-mediated suppression of miR-185. Our findings reveal the presence of the DC-SIGN-TCF1/LEF1-miR-185 loop in cancer cells with metastatic traits, implying that it may represent a new pathogenic mechanism of CRC metastasis. This character of the loop promises to provide new targets for blocking CRC invasive and metastatic activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Adhesion Molecules / physiology
  • Cell Line, Tumor
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology
  • Feedback, Physiological
  • Gene Expression Regulation, Neoplastic
  • Hepatocyte Nuclear Factor 1-alpha / metabolism
  • Humans
  • Lectins, C-Type / genetics
  • Lectins, C-Type / metabolism*
  • Lectins, C-Type / physiology
  • Lymphoid Enhancer-Binding Factor 1 / metabolism
  • Matrix Metalloproteinase 9 / metabolism
  • Mice, Inbred BALB C
  • Mice, Nude
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Neoplasm Invasiveness
  • Neoplasm Metastasis
  • Phosphatidylinositol 3-Kinases / metabolism
  • Prognosis
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Receptors, Cell Surface / physiology
  • Signal Transduction
  • Vascular Endothelial Growth Factor A / metabolism
  • beta Catenin / metabolism
  • src-Family Kinases / metabolism

Substances

  • Cell Adhesion Molecules
  • DC-specific ICAM-3 grabbing nonintegrin
  • HNF1A protein, human
  • Hepatocyte Nuclear Factor 1-alpha
  • LEF1 protein, human
  • Lectins, C-Type
  • Lymphoid Enhancer-Binding Factor 1
  • MIRN185 microRNA, human
  • MicroRNAs
  • Receptors, Cell Surface
  • Vascular Endothelial Growth Factor A
  • beta Catenin
  • lyn protein-tyrosine kinase
  • src-Family Kinases
  • Proto-Oncogene Proteins c-akt
  • Matrix Metalloproteinase 9