Developmental peculiarities in placentae of ovine uniparental conceptuses

PLoS One. 2017 Nov 30;12(11):e0188278. doi: 10.1371/journal.pone.0188278. eCollection 2017.

Abstract

Genomic imprinting is an epigenetic phenomenon regulating mono-allelic expression of genes depending on their parental origin. Defective genomic imprinting is involved in several placental disorders, such as intrauterine growth restriction and pre-eclampsia. Uniparental embryos, having maternal-only or paternal-only genomes (parthenogenotes [PAR] and androgenotes [AND], respectively), are useful models to study placentation. The aim of this work was to reveal the effect of parental genome (maternal and paternal) on placentation. To do this, uniparental (AND and PAR) and biparental (CTR) in vitro produced sheep embryos transferred to recipient females were collected at day 20 of pregnancy and their placentae were analyzed. qPCR analysis showed that imprinted genes (H19, IGF2R and DLK1) were expressed accordingly to their parental origin while the expression f DNA methyltransferases () was disregulated, especially in PAR (P < 0.05). AND placentae were significantly hypomethylated compared to both PAR and CTR (P = 0.023). Chorion-allantoid of AND showed impaired development of vessels and reduced mRNA expression of vasculogenetic factors (ANG2 P = 0.05; VEGFR2 P< 0.001; TIE2 P < 0.001). Morphologically, PAR placentae were characterized by abnormal structure of the trophoectodermal epithelium and reduced total number (P<0.03) of Trophoblastic Binucleate Cells. A reduced implantation rate of both classes of uniparental embryos (P<0.03) was also noted. Our results provide new insights into the characterization of uniparental embryos and demonstrate the complementary role of parental genomes for the correct establishment of pregnancy. Thus, our findings may suggest new targets to improve our understanding of the origin of imprinting-related placental dysfunction.

MeSH terms

  • Animals
  • DNA Methylation
  • Female
  • Genomic Imprinting
  • Placenta*
  • Pregnancy
  • Sheep / embryology*

Grants and funding

The research leading to these results received funding from the European Union’s Horizon 2020 Research and Innovation Programme under grant agreement No 692185 (Acronym ERAofART) and European Union Seventh Framework Programme for research, technological development and demonstration GA 312097 (Acronym FECUND) and the European Research Council Programme IDEAS GA 210103 (Acronym ANGIOPLACE) to GEP. This study was also partially financed by the Polish National Science Center GA 2015/19/D/NZ4/03696 to FZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.