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A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast.

In most mammalian species, a critical step of placenta development is the fusion of trophoblast cells into a multinucleated syncytiotrophoblast layer fulfilling essential fetomaternal exchange functions. Key insights into this process came from the discovery of envelope genes of retroviral origin, t... Full description

Journal Title: Proceedings of the National Academy of Sciences of the United States of America November 15, 2011, Vol.108(46), pp.E1164-E1173
Main Author: Dupressoir, Anne
Other Authors: Vernochet, Cécile , Harper, Francis , Guégan, Justine , Dessen, Philippe , Pierron, Gérard , Heidmann, Thierry
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1112304108
Link: http://search.proquest.com/docview/905667035/?pq-origsite=primo
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title: A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast.
format: Article
creator:
  • Dupressoir, Anne
  • Vernochet, Cécile
  • Harper, Francis
  • Guégan, Justine
  • Dessen, Philippe
  • Pierron, Gérard
  • Heidmann, Thierry
subjects:
  • Animals–Genetics
  • Epigenesis, Genetic–Metabolism
  • Female–Genetics
  • Gene Products, Env–Genetics
  • Genome–Metabolism
  • Humans–Metabolism
  • Mice–Metabolism
  • Mice, Knockout–Metabolism
  • Mice, Transgenic–Metabolism
  • Open Reading Frames–Metabolism
  • Placenta–Metabolism
  • Pregnancy–Metabolism
  • Pregnancy Proteins–Metabolism
  • Pregnancy, Animal–Metabolism
  • Rabbits–Metabolism
  • Retroviridae–Metabolism
  • Trophoblasts–Metabolism
  • Gene Products, Env
  • Pregnancy Proteins
  • Syncytin
  • Syncytin-A Protein, Mouse
  • Syncytin-B Protein, Mouse
ispartof: Proceedings of the National Academy of Sciences of the United States of America, November 15, 2011, Vol.108(46), pp.E1164-E1173
description: In most mammalian species, a critical step of placenta development is the fusion of trophoblast cells into a multinucleated syncytiotrophoblast layer fulfilling essential fetomaternal exchange functions. Key insights into this process came from the discovery of envelope genes of retroviral origin, the syncytins, independently acquired by the human (syncytin-1 and -2), mouse (syncytin-A and -B), and rabbit (syncytin-Ory1) genomes, with fusogenic properties and placenta-specific expression. We previously showed that mouse syncytin-A is essential for the formation of one of the two syncytiotrophoblast layers and for embryo survival. Here, we have generated syncytin-B KO mice and demonstrate that syncytin-B null placenta displays impaired formation of syncytiotrophoblast layer II (ST-II), with evidence of unfused apposed cells, and enlargement of maternal lacunae disrupting the placenta architecture. Unexpectedly, syncytin-B null embryos are viable, with only limited late-onset growth retardation and reduced neonate number. Microarray analyses identified up-regulation of the connexin 30 gene in mutant placentae, with the protein localized at the fetomaternal interface, suggesting gap junction-mediated compensatory mechanisms. Finally, double-KO mice demonstrate premature death of syncytin-A null embryos if syncytin-B is deleted, indicating cooperation between ST-I and ST-II. These findings establish that both endogenous retrovirus-derived syncytin genes contribute independently to the formation of the two syncytiotrophoblast layers during placenta formation, demonstrating a major role of retroviral gene capture, through convergent evolution, to generate multiple placental structures. Although some are absolutely required for completion of pregnancy, others are still amenable to "epigenetic" compensations, thus illustrating the complexity of the molecular machinery that developed during placental evolution. ; p. E1164-E1173.
language: eng
source:
identifier: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1112304108
fulltext: fulltext
issn:
  • 10916490
  • 1091-6490
url: Link


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titleA pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast.
creatorDupressoir, Anne ; Vernochet, Cécile ; Harper, Francis ; Guégan, Justine ; Dessen, Philippe ; Pierron, Gérard ; Heidmann, Thierry
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identifierE-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1112304108
subjectAnimals–Genetics ; Epigenesis, Genetic–Metabolism ; Female–Genetics ; Gene Products, Env–Genetics ; Genome–Metabolism ; Humans–Metabolism ; Mice–Metabolism ; Mice, Knockout–Metabolism ; Mice, Transgenic–Metabolism ; Open Reading Frames–Metabolism ; Placenta–Metabolism ; Pregnancy–Metabolism ; Pregnancy Proteins–Metabolism ; Pregnancy, Animal–Metabolism ; Rabbits–Metabolism ; Retroviridae–Metabolism ; Trophoblasts–Metabolism ; Gene Products, Env ; Pregnancy Proteins ; Syncytin ; Syncytin-A Protein, Mouse ; Syncytin-B Protein, Mouse
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descriptionIn most mammalian species, a critical step of placenta development is the fusion of trophoblast cells into a multinucleated syncytiotrophoblast layer fulfilling essential fetomaternal exchange functions. Key insights into this process came from the discovery of envelope genes of retroviral origin, the syncytins, independently acquired by the human (syncytin-1 and -2), mouse (syncytin-A and -B), and rabbit (syncytin-Ory1) genomes, with fusogenic properties and placenta-specific expression. We previously showed that mouse syncytin-A is essential for the formation of one of the two syncytiotrophoblast layers and for embryo survival. Here, we have generated syncytin-B KO mice and demonstrate that syncytin-B null placenta displays impaired formation of syncytiotrophoblast layer II (ST-II), with evidence of unfused apposed cells, and enlargement of maternal lacunae disrupting the placenta architecture. Unexpectedly, syncytin-B null embryos are viable, with only limited late-onset growth retardation and reduced neonate number. Microarray analyses identified up-regulation of the connexin 30 gene in mutant placentae, with the protein localized at the fetomaternal interface, suggesting gap junction-mediated compensatory mechanisms. Finally, double-KO mice demonstrate premature death of syncytin-A null embryos if syncytin-B is deleted, indicating cooperation between ST-I and ST-II. These findings establish that both endogenous retrovirus-derived syncytin genes contribute independently to the formation of the two syncytiotrophoblast layers during placenta formation, demonstrating a major role of retroviral gene capture, through convergent evolution, to generate multiple placental structures. Although some are absolutely required for completion of pregnancy, others are still amenable to "epigenetic" compensations, thus illustrating the complexity of the molecular machinery that developed during placental evolution. ; p. E1164-E1173.
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titleA pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast.
authorDupressoir, Anne ; Vernochet, Cécile ; Harper, Francis ; Guégan, Justine ; Dessen, Philippe ; Pierron, Gérard ; Heidmann, Thierry
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