Estrogen promotes progression of hormone-dependent breast cancer through CCL2-CCR2 axis by upregulation of Twist via PI3K/AKT/NF-κB signaling

Sci Rep. 2018 Jun 22;8(1):9575. doi: 10.1038/s41598-018-27810-6.

Abstract

The chemokine (C-C motif) ligand 2 (CCL2) with its cognate receptor chemokine (C-C motif) receptor 2 (CCR2) plays important roles in tumor invasion and metastasis. However, the mechanisms and mediators for autocrine CCL2 and CCL2-CCR2 axis remain elusive in breast cancer. Here we examined the levels of CCL2 in 4 breast cancer cell lines along with 57 human breast cancer specimens and found them significantly increased with presence of 17β-estradiol (E2) in estrogen receptor (ER)-positive breast cancer cells, while anti-estrogen treatment weakened this enhancement. CCL2 expression positively correlated with Twist staining and aggressiveness of breast cancer. Estrogen exposure facilitated the proliferation, invasion and metastasis of hormone-dependent breast cancer and promoted angiogenesis via the increased secretion of CCL2 in vitro and in vivo, which could be suppressed by disruption of CCL2-CCR2 axis with CCR2 antagonist RS102895. Knockdown of Twist in MCF-7 cells significantly inhibited E2-induced CCL2 production, indicating an essential role of Twist in CCL2 regulation under estrogenic condition. Our data show the hormonal regulation on CCL2-CCR2 axis is associated with enhanced Twist expression via activation of ERα and PI3K/AKT/NF-κB signaling. Thus, CCL2-CCR2 axis may represent as a novel therapeutic target eagerly needed for hormone-dependent breast cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Autocrine Communication / drug effects
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Chemokine CCL2 / metabolism*
  • Disease Progression
  • Estradiol / pharmacology
  • Estrogens / pharmacology*
  • Gene Knockdown Techniques
  • Human Umbilical Vein Endothelial Cells / cytology
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Humans
  • Mice
  • Middle Aged
  • NF-kappa B / metabolism
  • Neoplasm Invasiveness
  • Nuclear Proteins / deficiency
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Paracrine Communication / drug effects
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, CCR2 / metabolism*
  • Receptors, Estrogen / metabolism
  • Signal Transduction / drug effects*
  • Twist-Related Protein 1 / deficiency
  • Twist-Related Protein 1 / genetics
  • Twist-Related Protein 1 / metabolism*
  • Up-Regulation / drug effects*

Substances

  • Chemokine CCL2
  • Estrogens
  • NF-kappa B
  • Nuclear Proteins
  • Receptors, CCR2
  • Receptors, Estrogen
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • Estradiol
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt