An endogenous retroviral envelope syncytin and its cognate receptor identified in the viviparous placental Mabuya lizard

Abstract

Syncytins are envelope genes from endogenous retroviruses that have been captured during evolution for a function in placentation. They have been found in all placental mammals in which they have been searched, including marsupials. Placental structures are not restricted to mammals but also emerged in some other vertebrates, most frequently in lizards, such as the viviparous Scincidae. Here, we performed high-throughput RNA sequencing of a placenta transcriptome and screened for the presence of retroviral genes with a full-length ORF. We identified one such gene, which we named "," that has all the characteristics expected for a syncytin gene. It encodes a membrane-bound envelope protein with fusogenic activity ex vivo, is expressed at the placental level as revealed by in situ hybridization and immunohistochemistry, and is conserved in all species tested, spanning over 25 My of evolution. Its cognate receptor, required for its fusogenic activity, was searched for by a screening assay using the GeneBridge4 human/Chinese hamster radiation hybrid panel and found to be the MPZL1 gene, previously identified in mammals as a signal-transducing transmembrane protein involved in cell migration. Together, these results show that syncytin capture is not restricted to placental mammals, but can also take place in the rare nonmammalian vertebrates in which a viviparous placentotrophic mode of reproduction emerged. It suggests that similar molecular tools have been used for the convergent evolution of placentation in independently evolved and highly distant vertebrates.

Virus–Host Coevolution with a Focus on Animal and Human DNA Viruses

“…Retroviruses, for example, are so effective in genome integration and have been coevolving with vertebrates so long, that over 50% of the human genome was estimated to consist of endogenous retroviral elements (de Koning et al 2011). Some of these regions provide important and fundamental attributes to their integrator hosts, like the syncytin genes, which have an important role in placental development not only in various mammals but in viviparous lizards as well (Cornelis et al 2017;Imakawa and Nakagawa 2017). Other transposable elements contribute to embryonic development, stem cell pluripotency or cell differentiation in eukaryotes (Chuong et al 2017).…”

Decreased miR- 31 Suppress Cell Migration and Proliferation By Targeting Syncytin-1 in Pancreatic Carcinoma

“…More and more studies show that the critical roles of syncytin-1 in human diseases [22][23][24][25][26][27][28]. However, the functional role of syncytin-1 is complicated.…”

Convergent Co-option of the Retroviral gag Gene during the Early Evolution of Mammals

“…Retroviral env genes have been frequently captured and repurposed for placentation in placental mammals and the viviparous placental Mabuya lizard and are known as the syncytin genes (17,38,39). Syncytins arose independently more than 10 times in placental mammals (17,38,39). Moreover, a captured env gene was found to be conserved in spiny-rayed fishes (Acanthomorpha) for more than 110 million years (40).…”