Regulation of HBEGF by Micro-RNA for Survival of Developing Human Trophoblast Cells

PLoS One. 2016 Oct 4;11(10):e0163913. doi: 10.1371/journal.pone.0163913. eCollection 2016.

Abstract

Introduction: The growth factor HBEGF is upregulated post-transcriptionally in the low O2 environment of the human placenta during the first 10 weeks of pregnancy. We have examined the possible roles of HBEGF turnover and micro-RNA (miRNA) in its regulation by O2 in human first trimester trophoblast.

Methods: HTR-8/SVneo trophoblast cells were cultured at 2% or 20% O2. The cells were transfected with a dual luciferase reporter construct (psiCHECK-2) containing no insert (control), the HBEGF 3' untranslated region (3'UTR), or sub-regions of the 3'UTR, as well as with siRNA for DGCR8. RNA was extracted from trophoblast cells cultured at 2% O2 for 0-4 h for next-generation sequencing. HBEGF was quantified by ELISA. HBEGF, DGCR8, and β-actin were examined by western blotting.

Results: Protein turnover studies, using 10 μg/ml cyclohexamide, 1 μg/ml lactocystin, or 100 μg/ml MG132, demonstrated faster HBEGF degradation at 20% O2 than 2% O2, mediated by the proteasome. However, proteasome inhibition failed to initiate HBEGF accumulation at 20% O2. Reporter assays, comparing to empty vector, demonstrated that the intact HBEGF 3' UTR inhibited expression (0.26), while fragments containing only its flanking regions increased reporter activity (3.15; 3.43). No differential expression of miRNAs was found in trophoblast cells cultured at 2% and 20% O2. Nevertheless, HBEGF upregulation at 2% O2 was blocked when the miRNA-processing protein DGCR8 was silenced, suggesting a role for miRNA.

Conclusion: Our findings suggest involvement of flanking regions of the 3'UTR in activating HBEGF protein synthesis in response to 2% O2, possibly through a miRNA-mediated mechanism.

MeSH terms

  • Actins / metabolism
  • Cells, Cultured
  • Female
  • Gene Expression Regulation / drug effects
  • Heparin-binding EGF-like Growth Factor / genetics*
  • Heparin-binding EGF-like Growth Factor / metabolism
  • Humans
  • MicroRNAs
  • Oxygen / pharmacology*
  • Pregnancy
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Sequence Analysis, RNA / methods*
  • Trophoblasts / cytology*
  • Trophoblasts / drug effects
  • Trophoblasts / metabolism

Substances

  • Actins
  • DGCR8 protein, human
  • HBEGF protein, human
  • Heparin-binding EGF-like Growth Factor
  • MicroRNAs
  • RNA-Binding Proteins
  • Oxygen