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An Endogenous Retroviral Envelope Syncytin and Its Cognate Receptor Identified in the Viviparous Placental Mabuya Lizard

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An Endogenous Retroviral Envelope Syncytin and Its Cognate Receptor Identified in the Viviparous Placental Mabuya Lizard An endogenous retroviral envelope syncytin and its PNAS PLUS cognate receptor identified in the viviparous placental Mabuya lizard Guillaume Cornelisa,b,1,2, Mathis Funka,b,1, Cécile Vernocheta,b, Francisca Lealc,3, Oscar Alejandro Tarazonac,4, Guillaume Meuriced, Odile Heidmanna,b, Anne Dupressoira,b, Aurélien Mirallese, Martha Patricia Ramirez-Pinillac, and Thierry Heidmanna,b,5 SEE COMMENTARY aUnité Physiologie et Pathologie Moléculaires des Rétrovirus Endogènes et Infectieux, CNRS UMR 9196, Gustave Roussy, Villejuif, F-94805, France; bUMR 9196, Université Paris-Sud, Orsay, F-91405, France; cLaboratorio de Biologia Reproductiva de Vertebrados, Escuela de Biologia, Universidad Industrial de Santander, 680002 Bucaramanga, Colombia; dPlateforme de Bioinformatique, INSERM US23/CNRS UMS3655, Gustave Roussy, Villejuif, F-94805, France; and eInstitut de Systématique, Evolution, Biodiversité, Muséum National d’Histoire Naturelle, CNRS UPMC EPHE, Sorbonne Universités, Paris, F-75005, France Edited by R. Michael Roberts, University of Missouri-Columbia, Columbia, MO, and approved October 26, 2017 (received for review August 23, 2017) Syncytins are envelope genes from endogenous retroviruses that Remarkably, placental structures are not restricted to mamma- have been captured during evolution for a function in placentation. lian species. Placentation emerged independently and in a sto- They have been found in all placental mammals in which they have chastic manner in several groups of vertebrates, with the noticeable been searched, including marsupials. Placental structures are not exception of birds (reviewed in refs. 16 and 17). In particular, restricted to mammals but also emerged in some other vertebrates, complex placentas have been described in some South American most frequently in lizards, such as the viviparous Mabuya Scincidae. or African species of Scincidae lizards (18–21; reviewed in refs. 16, Here, we performed high-throughput RNA sequencing of a Mabuya 22, and 23). In one Scincidae genus, Mabuya, placental structures placenta transcriptome and screened for the presence of retroviral env form specialized regions very similar to those found in mammals, genes with a full-length ORF. We identified one such gene, which we e.g., the placentome where maternal and invasive fetal tissues are named “syncytin-Mab1,” that has all the characteristics expected for highly folded and interdigitated. Ultrastructural analysis of this a syncytin gene. It encodes a membrane-bound envelope protein with region further revealed the presence of a syncytial structure at the fusogenic activity ex vivo, is expressed at the placental level as materno–fetal interface, as observed in numerous mammalian revealed by in situ hybridization and immunohistochemistry, and is species. However, in contrast to most mammals, the syncytial layer conserved in all Mabuya species tested, spanning over 25 My of evo- of the Mabuya placenta is formed by maternal epithelial cells lution. Its cognate receptor, required for its fusogenic activity, was searched for by a screening assay using the GeneBridge4 human/Chi- Significance nese hamster radiation hybrid panel and found to be the MPZL1 gene, previously identified in mammals as a signal-transducing transmem- Retroviral envelope gene capture and exaptation for a placen- brane protein involved in cell migration. Together, these results show tal function has been demonstrated in mammals. Remarkably, that syncytin capture is not restricted to placental mammals, but can placental structures have also emerged on rare occasions in also take place in the rare nonmammalian vertebrates in which a vi- nonmammalian vertebrates, resulting in related modes of re- viparous placentotrophic mode of reproduction emerged. It suggests production. The Mabuya lizard, which emerged 25 Mya, pos- that similar molecular tools have been used for the convergent evo- sesses a placenta closely related to that of mammals. Here, lution of placentation in independently evolved and highly distant we identified a specific retroviral envelope gene capture that vertebrates. shows all the characteristic features of a bona fide mammalian syncytin, being conserved in Mabuya evolution, expressed in endogenous retrovirus | envelope protein | placenta | syncytin | receptor the placenta, and fusogenic. Together with the present identi- fication of its cognate receptor, these results show that syncytin yncytins are “captured” genes of retroviral origin that corre- capture is not restricted to mammals and is likely to be a major Sspond to the envelope gene of ancestrally endogenized retro- driving force for placenta emergence. viruses. These genes encode fusogenic proteins that are involved in the formation, by cell–cell fusion, of the syncytiotrophoblast at the Author contributions: G.C., M.F., and T.H. designed research; G.C., M.F., and C.V. per- placental materno–fetal interface in eutherian mammals (reviewed formed research; F.L., O.A.T., A.M., and M.P.R.-P. collected and processed live biological materials and samples; G.M. contributed analytic tools; G.C., M.F., C.V., G.M., O.H., A.D., in refs. 1 and 2). Furthermore, genetically modified mice in which A.M., M.P.R.-P., and T.H. analyzed data; and G.C., M.F., and T.H. wrote the paper. the two syncytin genes, syncytin-A and syncytin-B, were knocked out The authors declare no conflict of interest. showed deficiencies in placental development, with altered struc- This article is a PNAS Direct Submission. ture of the materno–fetal interface resulting in inhibition of growth Published under the PNAS license. or death of the embryo at midgestation (3, 4). Syncytins have been Data deposition: RNA sequencing data are deposited in the European Nucleotide Archive, found in all placental mammals in which they have been searched, www.ebi.ac.uk/ena (accession no. ERA1116158). Mabuya sequences described in this pa- with independently captured syncytins occurring across all major per (Mabuya MPZL1, syncytin-Mab1, and Mab-Env2–Mab-Env4) have been deposited in clades of placental mammals, including Euarchontoglires (primates, the GenBank database (accession nos. MG254887–MG254891, respectively). MICROBIOLOGY rodents, and lagomorphs), Laurasiatherians (ruminants and carni- See Commentary on page 13315. vores), Afrotherians (tenrec), and even Marsupials (opossum) (Fig. 1G.C. and M.F. contributed equally to this work. 1) (5–15). This has led to the proposal that these genes, which are 2Present address: Department of Genetics, Stanford University, Stanford, CA 94305. absolutely required for placentation as shown by the knockout mice 3Present address: Department of Biology, University of Florida, Gainesville, FL 32611. experiments, are most likely involved in the emergence and evo- 4Present address: Department of Molecular Genetics and Microbiology, University of lution of placental mammals from egg-laying animals (1). Analysis Florida, Gainesville, FL 32611. of the conservation of these genes further indicates that they have 5To whom correspondence should be addressed. Email: [email protected]. been subjected to purifying selection in the course of evolution, as This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. expected for any bona fide cellular gene. 1073/pnas.1714590114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1714590114 PNAS | Published online November 21, 2017 | E10991–E11000 Downloaded by guest on October 1, 2021 Tenrecidae Syn-Ten1 viously characterized as a membrane-bound signal transducer Proboscidae implicated in cell-migration processes (29–32). This identification Dasypodidae of a captured syncytin and its receptor in a distant viviparous lizard Bradypodidae with a placentotrophic mode of reproduction shows that syncytin Lagomorpha Syn-Ory1 capture is not restricted to mammals and is likely to be a major Rodentia Syn-A,-B,-Mar1 eutherian driving force for placenta emergence and evolution. Haplorrhini Syn-1, -2 mammals MAMMALIAN Strepsirrhini Results PLACENTA Ruminantia Syn-Rum1 High-Throughput Sequencing and in Silico Search for Retroviral Env Perissodactyla Genes Within the Mabuya Placental Transcriptome. Placental RNA Carnivora Syn-Car1 was extracted from pregnant Andean Mabuya sp. IV females cap- Insectivora tured in the wild (Methods). The transcriptome of a placenta at Didelphimorphia Syn-Opo1 marsupials embryonic development stage 35 (as defined in ref. 33), presenting Diprotodontia a well-established syncytium, was determined by the French National Monotremata Sequencing Center (Genoscope, Evry, France). Placental transcripts were assembled using de novo assembly methods in absence of Gallus gallus (chicken) birds a reference genome (Methods). Transcriptome reconstruction iden- Mabuya lizards tified 72,763 transcripts ranging from 123 bp to 24.4 kb [N50 (the Anolis carolinensis length N forwhich50%ofallbasesinthesequencesareinase- Danio rerio (zebrafish) quence of length L < N) = 2,869 bp; median size = 1.1 kb], 26,690 of Latimeria chalumnae bony fish (coelacanth) which (36.7%) could be positively matched to a known protein gene 50100150200250300350400 0 Mya from the Refseq Vertebrate database. A set of 21,253 transcripts shows significant expression (more than two tags per million) (34), Devonian CarboniferousPermianTriassic Jurassic Cretaceous Tertiary 16,398 of which were positively annotated (77.2%) and correspond to 13,189 unique genes, among which 10,079 were nonhousekeeping genes. This subset of transcripts contains a range of genes annotated as
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