The CCR2 3'UTR functions as a competing endogenous RNA to inhibit breast cancer metastasis

J Cell Sci. 2017 Oct 1;130(19):3399-3413. doi: 10.1242/jcs.202127. Epub 2017 Aug 17.

Abstract

Diverse RNA transcripts acting as competing endogenous RNAs (ceRNAs) can co-regulate each other's expression by competing for shared microRNAs. CCR2 protein, the receptor for CCL2, is implicated in cancer progression. However, we found that a higher CCR2 mRNA level is remarkably associated with prolonged survival of breast cancer patients. These conflicting results prompted us to study the non-coding function of CCR2 mRNA. We found that the CCR2 3' untranslated region (UTR) inhibited MDA-MB-231 and MCF-7 cell metastasis by repressing epithelial-mesenchymal transition (EMT) in vitro, and suppressed breast cancer metastasis in vivo Mechanistically, the CCR2 3'UTR modulated the expression of the RhoGAP protein STARD13 via acting as a STARD13 ceRNA in a microRNA-dependent and protein coding-independent manner. The CCR2 3'UTR blocked the activation of RhoA-ROCK1 pathway, which is the downstream effector of STARD13, and thus decreased the phosphorylation level of myosin light chain 2 (MLC2) and formation of F-actin. Additionally, the function of the CCR2 3'UTR was dependent on STARD13 expression. In conclusion, our results confirmed that the CCR2 3'UTR acts as a metastasis suppressor by acting as a ceRNA for STARD13 and thus inhibiting RhoA-ROCK1-MLC-F-actin pathway in breast cancer cells.This article has an associated First Person interview with the first author of the paper.

Keywords: 3′UTR; Breast cancer; CCR2; Metastasis; ceRNA.

MeSH terms

  • 3' Untranslated Regions*
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Female
  • GTPase-Activating Proteins / genetics
  • GTPase-Activating Proteins / metabolism
  • Humans
  • MCF-7 Cells
  • Neoplasm Metastasis
  • RNA, Neoplasm / genetics
  • RNA, Neoplasm / metabolism*
  • Receptors, CCR2 / genetics
  • Receptors, CCR2 / metabolism*
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • rho-Associated Kinases / genetics
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein / genetics
  • rhoA GTP-Binding Protein / metabolism

Substances

  • 3' Untranslated Regions
  • CCR2 protein, human
  • GTPase-Activating Proteins
  • RNA, Neoplasm
  • Receptors, CCR2
  • STARD13 protein, human
  • Tumor Suppressor Proteins
  • rho GTPase-activating protein
  • RHOA protein, human
  • ROCK1 protein, human
  • rho-Associated Kinases
  • rhoA GTP-Binding Protein