Novel lncRNA-HZ04 promotes BPDE-induced human trophoblast cell apoptosis and miscarriage by upregulating IP3 R1 /CaMKII/SGCB pathway by competitively binding with miR-hz04

FASEB J. 2021 Sep;35(9):e21789. doi: 10.1096/fj.202100376RR.

Abstract

Normal pregnancy is essential for human reproduction. However, BaP (benzo(a)pyrene) and its metabolite BPDE (benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide) could cause dysfunctions of human trophoblast cells and might further induce miscarriage. Yet, the underlying mechanisms remain largely unknown. Herein, we identified a novel upregulated lnc-HZ04 and a novel downregulated miR-hz04 in villous tissues of unexplained recurrent miscarriage (RM) relative to those in healthy control tissues and also in BPDE-treated human trophoblast cells. Lnc-HZ04 directly and specifically bound with miR-hz04, diminished the reduction effects of miR-hz04 on IP3 R1 mRNA expression level and on IP3 R1 mRNA stability, and then activated the Ca2+ -mediated IP3 R1 /p-CaMKII/SGCB pathway, which further promoted trophoblast cell apoptosis. The miR-hz04 target site on lnc-HZ04 played crucial roles in these regulations. In normal trophoblast, relatively less lnc-HZ04 and more miR-hz04 suppressed this apoptosis pathway and gave normal pregnancy. After exposure to BPDE or in RM tissues, p53 was upregulated, which might promote p53-mediated lnc-HZ04 transcription. Relatively more lnc-HZ04 and less miR-hz04 activated this apoptosis pathway and might further induce miscarriage. BaP could also induce mice miscarriage by upregulating its corresponding murine apoptosis pathway. Therefore, BPDE-induced apoptosis of human trophoblast cells was associated with the occurrence of miscarriage. This work discovered the regulation roles of lnc-HZ04 and miR-hz04 and provided scientific and clinical understanding of the occurrence of unexplained miscarriage.

Keywords: IP3R1/Ca2+/CaMKII/SGCB; competing endogenous RNAs (ceRNAs); environmental BaP or BPDE; female trophoblast cell apoptosis; miscarriage or spontaneous abortion; noncoding lncRNA-HZ04 and miR-hz04.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 7,8-Dihydro-7,8-dihydroxybenzo(a)pyrene 9,10-oxide / pharmacology
  • Abortion, Habitual / drug therapy
  • Abortion, Habitual / genetics*
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Cell Line
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Female
  • Humans
  • Inositol 1,4,5-Trisphosphate Receptors / genetics
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics*
  • Pregnancy
  • RNA, Long Noncoding / genetics*
  • Sarcoglycans / genetics
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Trophoblasts / drug effects
  • Trophoblasts / metabolism*
  • Up-Regulation / drug effects
  • Up-Regulation / genetics*

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • MicroRNAs
  • RNA, Long Noncoding
  • Sarcoglycans
  • 7,8-Dihydro-7,8-dihydroxybenzo(a)pyrene 9,10-oxide
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2