Bovine Trophoblastic Cell Differentiation and Binucleation Involves Enhanced Endogenous Retrovirus Element Expression.

Koshi, K.; Suzuki, Yasunori; Nakaya, Yuki; Imai, Kyoichi; Hosoe, Misa; Takahashi, Toshio; Kizaki, Keiichiro; Miyazawa, Takayuki; Hashizume, Kazuyoshi

doi:10.1093/biolreprod/87.s1.379

Cited by 4 publications

(7 citation statements)

References 33 publications

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“…3). Interestingly, two of the families, Bos-Env4 and Bos-Env5, correspond to previously identified sequences (23,24); the other three families had not been described previously. Analysis of the overall structure of the five identified Env families (Figs.…”

Section: In Silico Search For Retroviral Env Genes Within the Cow (Bosupporting

confidence: 55%

“…Both the bos-env1 orthol- (Table S2). Bos-Env4 and BosEnv5 (chr24) correspond to the Env of the previously identified bovine ERVs BERV-K1 and -K2 (23,24), respectively. BFV, bovine foamy virus; BLV, bovine leukemia virus; ENTV, enzootic tumorigenic virus; FeLV, feline leukemia virus; JSRV, Jaagsiekte retrovirus; HERV, human ERV; HFV, human foamy virus; HIV, human immunodeficiency virus; MoMLV, Moloney murine leukemia virus; mIAPE, Mus musculus intracisternal A-type particle with an envelope gene; MMTV, murine mammary tumor virus; MPMV, Mason-Pfizer monkey virus; OMVV, ovine Maedi-Visna virus; PERV, porcine ERV.…”

Section: In Silico Search For Retroviral Env Genes Within the Cow (Bomentioning

confidence: 97%

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Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants

Cornelis

Heidmann

Degrelle

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

131

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Syncytins are envelope genes of retroviral origin that have been coopted for a role in placentation and likely contribute to the remarkable diversity of placental structures. Independent capture events have been identified in primates, rodents, lagomorphs, and carnivores, where they are involved in the formation of a syncytium layer at the fetomaternal interface via trophoblast cell-cell fusion. We searched for similar genes within the suborder Ruminantia where the placenta lacks an extended syncytium layer but displays a heterologous cell-fusion process unique among eutherian mammals. An in silico search for intact envelope genes within the Bos taurus genome identified 18 candidates belonging to five endogenous retrovirus families, with one gene displaying both placenta-specific expression, as assessed by quantitative RT-PCR analyses of a large panel of tissues, and conservation in the Ovis aries genome. Both the bovine and ovine orthologs displayed fusogenic activity by conferring infectivity on retroviral pseudotypes and triggering cell-cell fusion. In situ hybridization of placenta sections revealed specific expression in the trophoblast binucleate cells, consistent with a role in the formation-by heterologous cell fusion with uterine cells-of the trinucleate cells of the cow and the syncytial plaques of the ewe. Finally, we show that this gene, which we named "Syncytin-Rum1," is conserved among 16 representatives of higher ruminants, with evidence for purifying selection and conservation of its fusogenic properties, over 30 millions years of evolution. These data argue for syncytins being a major driving force in the emergence and diversity of the placenta.synepitheliochorial | placental evolution | phylogeny | placentome | ERV

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Section: In Silico Search For Retroviral Env Genes Within the Cow (Bosupporting

confidence: 55%

Section: In Silico Search For Retroviral Env Genes Within the Cow (Bomentioning

confidence: 97%

Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants

Cornelis

Heidmann

Degrelle

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

131

View full text Add to dashboard Cite

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“…Current hypothesis supports that syncytin-Rum1 was integrated into ruminant genomes 20 MYA while Fematrin-1 was integrated into the bovine genome 11 MYA [94]. As for bERVE-A, its mRNA is found only in binucleate cells throughout the gestation period, and this gene contains syncytin 1-like SU domain and ASCT2 binding domain; however, it does not possess fusogenic activity due to a loss of the fusion peptide [76]. Furthermore, the integration of BERV-P was recently found in ruminants [95].…”

Section: Endogenous Retroviruses and Pregnancymentioning

confidence: 53%

“…Evidence has accumulated that ERVs are now realized as factors implicated in development and differentiation of TE cells in mammalian species such as humans, rodents, dogs/cats, rabbits, sheep, cattle, tenrecs and opossums [70][71][72][73][74][75][76][77][78]. During the course of evolution, all vertebrates have been exposed to multiple waves of cross-species infection by exogenous retroviruses, some of which infected germ cells and have been inherited in an integrated, proviral form [79].…”

Section: Endogenous Retroviruses and Pregnancymentioning

confidence: 99%

Conceptus implantation and placentation: molecules related to epithelial–mesenchymal transition, lymphocyte homing, endogenous retroviruses, and exosomes

Imakawa

Bai

Fujiwara

et al. 2015

Reprod Medicine & Biology

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Processes of conceptus implantation and placentation, unique to mammalian reproduction, have been extensively studied. It was once thought that processes of these events varied greatly, notably between invasive and noninvasive modes of implantation and/or placentation. Regardless of the mode of implantation, however, physiological and biochemical processes in conceptus implantation to the maternal endometrium including the kinds of gene expression and their products are now considered not to differ so much. Recent progress has identified that in addition to the hormones, cytokines, proteases and cell adhesion molecules classically characterized, epithelial-mesenchymal transition, molecules related to lymphocyte homing, the expression of endogenous retroviruses and possibly exosomes are all required for the progression of conceptus implantation to placentation. In this review, therefore, new findings related to these events are integrated into the context of conceptus implantation to the maternal endometrium.

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“…We recently reported that the BERV‐K1 Env , fematrin‐1 , is conserved in the genome of the Bovinae species and that it is specifically expressed in BNCs of the placenta and exhibits fusogenic activity, using different types of cells, except for trophoblast cells, in vitro (Baba et al ; Koshi et al ; Nakaya et al ). However, there is no direct evidence regarding whether fematrin‐1 possesses fusogenic activity in trophoblast cells.…”

Section: Introductionmentioning

confidence: 99%

Induction of ovine trophoblast cell fusion by fematrin‐1 in vitro

Koshi

Nakaya

Kizaki

et al. 2015

Animal Science Journal

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Endogenous retroviruses present in the genomes take a specific role in placental formation in various vertebrates, including bovine and sheep. Fematrin-1, which is the envelope (Env) protein of bovine endogenous retrovirus found in bovine placenta, is involved in the formation of fetomaternal hybrid cells in cattle placenta. This study was conducted to clarify whether fematrin-1 possesses fusogenic activity in trophoblast cells. Another question is whether Env proteins only have species-specific activity or not. For this, fematrin-1 gene was transfected in ovine trophoblast cells, and we examined fusogenic activity with Cos-7 cells. Although fematrin-1 fusogenic activity was detected in both neutral and acidic pH conditions, acidic condition significantly enhanced it. These activities were rather weaker than those of vesicular stomatitis virus G protein as a positive control. However, the ratio of fematrin-1 and vesicular stomatitis virus G protein fusion index was confirmed similar to those in the previous reports. Some fusion cells showed multinucleate cells. These results imply that fematrin-1 is involved in the formation of trophoblast hybrid cells even in different species trophoblastic cells.

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Bovine Trophoblastic Cell Differentiation and Binucleation Involves Enhanced Endogenous Retrovirus Element Expression.

Cited by 4 publications

References 33 publications

Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants

Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants

Conceptus implantation and placentation: molecules related to epithelial–mesenchymal transition, lymphocyte homing, endogenous retroviruses, and exosomes

Induction of ovine trophoblast cell fusion by fematrin‐1 in vitro

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