RBM38 is involved in TGF-β-induced epithelial-to-mesenchymal transition by stabilising zonula occludens-1 mRNA in breast cancer

Br J Cancer. 2017 Aug 22;117(5):675-684. doi: 10.1038/bjc.2017.204. Epub 2017 Jul 6.

Abstract

Background: The transforming growth factor-β (TGF-β) pathway plays a vital role in driving cancer cell epithelial-mesenchymal transition (EMT). Zonula occludens-1 (ZO-1), which is downregulated in response to TGF-β, is able to control endothelial cell-cell tension, cell migration, and barrier formation. However, the molecular mechanism of how TGF-β regulates ZO-1 expression remains unclear.

Methods: Breast cancer cells were treated with TGF-β to induce an EMT progress. Chromatin immunoprecipitation and dual-luciferase reporter assay were performed to investigate direct relationship between Snail and RNA binding motif protein 38 (RBM38). The RNA immunoprecipitation combined with RNA electrophoretic mobility shift assay and dual-luciferase reporter assay were conducted to testify direct relationship between RBM38 and ZO-1. The ZO-1 siRNA was transfected to breast cancer cells that overexpress RBM38 and the control, followed by transwell and Matrigel invasion assays to examine cell migratory and invasive ability.

Results: Transforming growth factor-β induced a remarkable downregulation of RBM38 in breast cancer that was directly regulated by transcription repressor Snail targeting the E-box elements in promoter region of RBM38 gene. Additionally, RBM38 positively regulated ZO-1 transcript via directly binding to AU/U-rich elements in its mRNA 3'-UTR. Moreover, by magnifying RBM38 expression, cell migration and invasion mediated by knockdown of ZO-1 in breast cancer were reversed.

Conclusions: All the results clarified a linear regulation relationship among Snail, RBM38, and ZO-1, implicating RBM38 as a pivotal mediator in TGF-β-induced EMT in breast cancer.

MeSH terms

  • 3' Untranslated Regions
  • Benzamides / pharmacology
  • Breast Neoplasms / chemistry
  • Cell Movement / drug effects
  • Cell Movement / genetics
  • Dioxoles / pharmacology
  • Down-Regulation
  • E-Box Elements / genetics
  • Epithelial-Mesenchymal Transition* / drug effects
  • Female
  • Gene Expression
  • Humans
  • MCF-7 Cells
  • Promoter Regions, Genetic
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • RNA, Messenger / metabolism*
  • RNA, Small Interfering / genetics
  • RNA-Binding Proteins / analysis
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism*
  • Receptor, Transforming Growth Factor-beta Type I
  • Receptors, Transforming Growth Factor beta / antagonists & inhibitors
  • Snail Family Transcription Factors / genetics
  • Transfection
  • Transforming Growth Factor beta / pharmacology
  • Zonula Occludens-1 Protein / analysis
  • Zonula Occludens-1 Protein / genetics*
  • Zonula Occludens-1 Protein / metabolism*

Substances

  • 3' Untranslated Regions
  • 4-(5-benzo(1,3)dioxol-5-yl-4-pyridin-2-yl-1H-imidazol-2-yl)benzamide
  • Benzamides
  • Dioxoles
  • RBM38 protein, human
  • RNA, Messenger
  • RNA, Small Interfering
  • RNA-Binding Proteins
  • Receptors, Transforming Growth Factor beta
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Transforming Growth Factor beta
  • Zonula Occludens-1 Protein
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type I