Epigenetic down regulation of G protein-coupled estrogen receptor (GPER) functions as a tumor suppressor in colorectal cancer

Mol Cancer. 2017 May 5;16(1):87. doi: 10.1186/s12943-017-0654-3.

Abstract

Background: Estrogenic signals are suggested to have protection roles in the development of colorectal cancer (CRC). The G protein-coupled estrogen receptor (GPER) has been reported to mediate non-genomic effects of estrogen in hormone related cancers except CRC. Its expression and functions in CRC were investigated.

Methods: The expression of GPER and its associations with clinicopathological features were examined. The mechanisms were further investigated using cells, mouse xenograft models, and clinical human samples.

Results: GPER was significantly (p < 0.01) down regulated in CRC tissues compared with their matched adjacent normal tissues in our two cohorts and three independent investigations from Oncomine database. Patients whose tumors expressing less (n = 36) GPER showed significant (p < 0.01) poorer survival rate as compared with those with greater levels of GPER (n = 54). Promoter methylation and histone H3 deacetylation were involved in the down regulation of GPER in CRC cell lines and clinical tissues. Activation of GPER by its specific agonist G-1 inhibited proliferation, induced cell cycle arrest, mitochondrial-related apoptosis and endoplasmic reticulum (ER) stress of CRC cells. The upregulation of reactive oxygen species (ROS) induced sustained ERK1/2 activation participated in G-1 induced cell growth arrest. Further, G-1 can inhibit the phosphorylation, nuclear localization, and transcriptional activities of NF-κB via both canonical IKKα/ IκBα pathways and phosphorylation of GSK-3β. Xenograft model based on HCT-116 cells confirmed that G-1 can suppress the in vivo progression of CRC.

Conclusions: Epigenetic down regulation of GPER acts as a tumor suppressor in colorectal cancer and its specific activation might be a potential approach for CRC treatment.

Keywords: CRC; G-1; GPER; NF-κB; ROS.

MeSH terms

  • Aged
  • Animals
  • Apoptosis / drug effects
  • Cell Cycle Checkpoints / drug effects
  • Cell Proliferation / drug effects
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / pathology
  • Cyclopentanes / administration & dosage
  • Epigenesis, Genetic / genetics*
  • Estrogens / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • HCT116 Cells
  • Humans
  • MAP Kinase Signaling System / drug effects
  • Male
  • Mice
  • Middle Aged
  • Neoplasms, Hormone-Dependent / genetics*
  • Neoplasms, Hormone-Dependent / pathology
  • Quinolines / administration & dosage
  • Reactive Oxygen Species / metabolism
  • Receptors, Estrogen / genetics*
  • Receptors, G-Protein-Coupled / genetics*
  • Xenograft Model Antitumor Assays

Substances

  • 1-(4-(6-bromobenzo(1,3)dioxol-5-yl)-3a,4,5,9b-tetrahydro-3H-cyclopenta(c)quinolin-8-yl)ethanone
  • Cyclopentanes
  • Estrogens
  • GPER1 protein, human
  • Quinolines
  • Reactive Oxygen Species
  • Receptors, Estrogen
  • Receptors, G-Protein-Coupled