Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials

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

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Gene Expression Profiling
  • Gene Products, env / genetics*
  • Genes, env
  • In Situ Hybridization
  • Marsupialia / classification
  • Marsupialia / genetics*
  • Molecular Sequence Data
  • Phylogeny
  • Placenta / physiology*
  • Pregnancy
  • Pregnancy Proteins / genetics*
  • Retroviridae / physiology*
  • Transcription, Genetic
  • Viral Envelope Proteins / genetics*

Substances

  • Gene Products, env
  • Pregnancy Proteins
  • Viral Envelope Proteins
  • syncytin

Associated data

  • GENBANK/KM235324
  • GENBANK/KM235325
  • GENBANK/KM235326
  • GENBANK/KM235327
  • GENBANK/KM235328
  • GENBANK/KM235329
  • GENBANK/KM235330
  • GENBANK/KM235331
  • GENBANK/KM235332
  • GENBANK/KM235333
  • GENBANK/KM235334
  • GENBANK/KM235335
  • GENBANK/KM235336
  • GENBANK/KM235337
  • GENBANK/KM235338
  • GENBANK/KM235339
  • GENBANK/KM235340
  • GENBANK/KM235341
  • GENBANK/KM235342
  • GENBANK/KM235343
  • GENBANK/KM235344
  • GENBANK/KM235345
  • GENBANK/KM235346
  • GENBANK/KM235347
  • GENBANK/KM235348
  • GENBANK/KM235349
  • GENBANK/KM235350
  • GENBANK/KM235351
  • GENBANK/KM235352
  • GENBANK/KM235353
  • GENBANK/KM235354
  • GENBANK/KM235355
  • GENBANK/KM235356
  • GENBANK/KM235357
  • GENBANK/KM235358
  • GENBANK/KM235359