Differential regulation of sFlt-1 splicing by U2AF65 and JMJD6 in placental-derived and endothelial cells

Biosci Rep. 2020 Feb 28;40(2):BSR20193252. doi: 10.1042/BSR20193252.

Abstract

Despite years of study, the gestational disorder preeclampsia (PE) remains poorly understood. One proposed mechanism of PE development is increased soluble VEGF receptor-1 (sFlt-1), ultimately causing angiogenic imbalance and endothelial dysfunction. The soluble protein is an alternative splice variant of FLT1, which also encodes for the full-length receptor Flt-1. The mechanism of the alternative splicing, and the reason for its inappropriate increase in preeclampsia, is not well understood. U2 auxiliary factor 65 (U2AF65) and jumonji C domain-containing protein 6 (JMJD6) have been implicated in the splicing of sFlt-1. Using siRNA knockdown and plasmid overexpression in immortalized placental trophoblasts (BeWo) and primary endothelial cells (HUVECs), we examined the role these proteins play in production of sFlt-1. Our results showed that U2AF65 has little, if any, effect on sFlt-1 splicing, and JMJD6 may enhance sFlt-1 splicing, but is not necessary for splicing to occur. Utilizing a hypoxic environment to mimic conditions of the preeclamptic placenta, as well as examining placentae in the reduced uterine perfusion pressure (RUPP) model of PE, which exhibits increased circulating sFlt-1, we found increased expression of JMJD6 in both hypoxic cells and placental tissue. Additionally, we observed a potential role for U2AF65 and JMJD6 to regulate the extracellular matrix enzyme heparanase, which may be involved in the release of sFlt-1 protein from the extracellular matrix. It will be important to study the role of these proteins in different tissues in the future, as changes in expression had differential effects on sFlt-1 splicing in the different cell types studied here.

Keywords: JMJD6; U2AF65; alternative splicing; preeclampsia; sFlt-1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing*
  • Animals
  • Cell Hypoxia
  • Cell Line
  • Disease Models, Animal
  • Female
  • Glucuronidase / metabolism
  • Human Umbilical Vein Endothelial Cells / enzymology*
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Pre-Eclampsia / enzymology*
  • Pre-Eclampsia / genetics
  • Pre-Eclampsia / physiopathology
  • Pregnancy
  • Rats, Sprague-Dawley
  • Splicing Factor U2AF / genetics
  • Splicing Factor U2AF / metabolism*
  • Trophoblasts / enzymology*
  • Vascular Endothelial Growth Factor Receptor-1 / genetics
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism*

Substances

  • Splicing Factor U2AF
  • U2AF2 protein, human
  • JMJD6 protein, human
  • Jmjd6 protein, rat
  • Jumonji Domain-Containing Histone Demethylases
  • FLT1 protein, human
  • Flt1 protein, rat
  • Vascular Endothelial Growth Factor Receptor-1
  • heparanase
  • Glucuronidase