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Proc Natl Acad Sci U S A. 2015 Feb 3;112(5):E487-96. doi: 10.1073/pnas.1417000112. Epub 2015 Jan 20.

Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials.

Author information

1
Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France; Université Paris Denis Diderot, Sorbonne Paris-Cité, Paris, F-75013, France;
2
Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
3
Zooparc de Beauval et Beauval Nature, Saint Aignan, F-41110, France;
4
Laboratoire de Paléontologie, Phylogénie et Paléobiologie, UMR 5554 CNRS, Université Montpellier II, Montpellier, F-34095, France;
5
LOEWE Biodiversity and Climate Research Center, Frankfurt am Main, D-60325 Germany;
6
Department of Zoology, University of Melbourne, Melbourne, VIC 3010, Australia; and.
7
Systematic Zoology, Humboldt University, 10099 Berlin, Germany.
8
Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France; heidmann@igr.fr.

Abstract

Syncytins are genes of retroviral origin captured by eutherian mammals, with a role in placentation. Here we show that some marsupials-which are the closest living relatives to eutherian mammals, although they diverged from the latter ∼190 Mya-also possess a syncytin gene. The gene identified in the South American marsupial opossum and dubbed syncytin-Opo1 has all of the characteristic features of a bona fide syncytin gene: It is fusogenic in an ex vivo cell-cell fusion assay; it is specifically expressed in the short-lived placenta at the level of the syncytial feto-maternal interface; and it is conserved in a functional state in a series of Monodelphis species. We further identify a nonfusogenic retroviral envelope gene that has been conserved for >80 My of evolution among all marsupials (including the opossum and the Australian tammar wallaby), with evidence for purifying selection and conservation of a canonical immunosuppressive domain, but with only limited expression in the placenta. This unusual captured gene, together with a third class of envelope genes from recently endogenized retroviruses-displaying strong expression in the uterine glands where retroviral particles can be detected-plausibly correspond to the different evolutionary statuses of a captured retroviral envelope gene, with only syncytin-Opo1 being the present-day bona fide syncytin active in the opossum and related species. This study would accordingly recapitulate the natural history of syncytin exaptation and evolution in a single species, and definitely extends the presence of such genes to all major placental mammalian clades.

KEYWORDS:

endogenous retrovirus; envelope protein; fusogenic activity; marsupials; syncytiotrophoblast

PMID:
25605903
PMCID:
PMC4321253
DOI:
10.1073/pnas.1417000112
[Indexed for MEDLINE]
Free PMC Article

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