PTGER3 induces ovary tumorigenesis and confers resistance to cisplatin therapy through up-regulation Ras-MAPK/Erk-ETS1-ELK1/CFTR1 axis

EBioMedicine. 2019 Feb:40:290-304. doi: 10.1016/j.ebiom.2018.11.045. Epub 2019 Jan 14.

Abstract

Background: Inflammatory mediator prostaglandin E2-prostaglandin E2 receptor EP3 (PTGER3) signaling is critical for tumor-associated angiogenesis, tumor growth, and chemoresistance. However, the mechanism underlying these effects in ovarian cancer is not known.

Methods: An association between higher tumoral expression of PTGER3 and shorter patient survival in the ovarian cancer dataset of The Cancer Genome Atlas prompted investigation of the antitumor effects of PTGER3 downmodulation. PTGER3 mRNA and protein levels were higher in cisplatin-resistant ovarian cancer cells than in their cisplatin-sensitive counterparts.

Findings: Silencing of PTGER3 via siRNA in cancer cells was associated with decreased cell growth and less invasiveness, as well as cell-cycle arrest and increased apoptosis, mediated through the Ras-MAPK/Erk-ETS1-ELK1/CFTR1 axis. Furthermore, sustained PTGER3 silencing with multistage vector and liposomal 2'-F-phosphorodithioate-siRNA-mediated silencing of PTGER3 combined with cisplatin resulted in robust antitumor effects in cisplatin-resistant ovarian cancer models.

Interpretation: These findings identify PTGER3 as a potential therapeutic target in chemoresistant ovarian cancers expressing high levels of this oncogenic protein. FUND: National Institutes of Health/National Cancer Institute, USA.

Keywords: CFTR; Chemically modified siRNA; Cisplatin resistance; ELK1; ETS1; Ovarian cancer; PTGER3; RNA interference.

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Biomarkers
  • Cell Cycle / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Transformation, Neoplastic / genetics*
  • Cell Transformation, Neoplastic / metabolism
  • Cisplatin / pharmacology*
  • Drug Resistance, Neoplasm / genetics*
  • Female
  • Gene Knockdown Techniques
  • Gene Silencing
  • Humans
  • Immunohistochemistry
  • Models, Biological
  • Ovarian Neoplasms / drug therapy
  • Ovarian Neoplasms / etiology*
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / pathology
  • Proto-Oncogene Protein c-ets-1 / metabolism
  • Receptors, Prostaglandin E, EP3 Subtype / genetics*
  • Receptors, Prostaglandin E, EP3 Subtype / metabolism
  • Signal Transduction / drug effects*

Substances

  • Antineoplastic Agents
  • Biomarkers
  • ETS1 protein, human
  • PTGER3 protein, human
  • Proto-Oncogene Protein c-ets-1
  • Receptors, Prostaglandin E, EP3 Subtype
  • Cisplatin