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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 51; pp. E10991 - E11000
• Main Authors: Cornelis, Guillaume, Funk, Mathis, Vernochet, Cécile, Leal, Francisca, Tarazona, Oscar Alejandro, Meurice, Guillaume, Heidmann, Odile, Dupressoir, Anne, Miralles, Aurélien, Ramirez-Pinilla, Martha Patricia, Heidmann, Thierry
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 19.12.2017
• Series: From the Cover
• Subjects: Biological evolution; Biological Sciences; Cell migration; Endogenous retroviruses; Evolutionary genetics; Gene expression; Gene sequencing; Genes; Hybridization; Immunohistochemistry; Lizards; Mabuya; Mammals; Marsupials; Membrane proteins; Placenta; PNAS Plus; Ribonucleic acid; RNA; Scincidae; Signal transduction; Syncytin; Vertebrates; Viral envelope proteins; syncytin; placenta; receptor; envelope protein; endogenous retrovirus
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1714590114

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 Mabuya Scincidae. Here, we performed high-throughput RNA sequencing of a Mabuya placenta transcriptome and screened for the presence of retroviral env genes with a full-length ORF. We identified one such gene, which we named “syncytin-Mab1,” 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 Mabuya 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.