Functional specialization in the ruminant placenta: Evidence for two populations of fetal binucleate cells of different selective synthetic capacity

Wooding, F. B. P.; Morgan, Gilbert T.; Monaghan, Sean J.; Hamon, M.; Heap, R. B.

doi:10.1016/s0143-4004(05)80646-0

Cited by 68 publications

(64 citation statements)

References 18 publications

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“…The expression of Dkk-1 mRNA in cotyledon tissue was localised to the BNCs. The BNCs comprise of about 20% of the trophoblast cells at the fetal-maternal interface and there is evidence in sheep that although placental lactogen protein is produced in all BNCs, a specific binucleate U3 (SBU3) protein was found only in cotyledonary BNCs [33]. We have discovered that a subset of the Day 50 cotyledonary BNCs, identified with bPL antibody, also contained Dkk-1 protein, showing that bovine BNCs are also comprised of populations of cells with different properties.…”

Section: Discussionmentioning

confidence: 81%

Dickkopf-1 Expression During Early Bovine Placentation and Its Down-regulation in Somatic Cell Nuclear Transfer (SCNT) Pregnancies

Ledgard

Lee

Couldrey

et al. 2009

Journal of Reproduction and Development

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Abstract. The precise role of Dickkopf-1 (Dkk-1) during early bovine trophoblast development and subsequent placentation is not fully understood. Using somatic cell nuclear transfer (SCNT) generated pregnancies as a model of poor placentation we have found that mean levels of Dkk-1 mRNA were 1.5 fold lower in SCNT fetal cotyledon tissue at Day 50 of gestation than those resulting from artificial insemination (AI) and 2 fold lower at Days 100 and 150 (P<0.004). Dkk-1 expression in cotyledon tissue was localized by in situ hybridization to fetal binucleate cells (BNCs). Examining conceptuses from blastocyst stage we show that Dkk-1 mRNA was first evident between Days 15-20 of gestation in trophoblast tissue (when BNCs first appear) prior to the initial expression of the BNC specific bovine placental lactogen (bPL) on Day 20. Dkk-1 mRNA levels were higher than bPL in trophoblast tissue throughout the pre-attachment period (Days 24-31), however, this reversed during cotyledon development with only a subset of the bPL immunoreactive BNCs also containing Dkk-1 protein, suggesting a specific role for Dkk-1 during early placentation. One function of Dkk-1 is as an antagonist of the Wnt signaling pathway and, although Wnt5A and Wnt7A mRNAs were expressed in Day 50 bovine cotyledons, their expression levels were similar between AI and SCNT. In addition, the nuclear localization of β-catenin, which is an indicator of activation of the Wnt pathway, was also similar between AI and SCNT cotyledon tissue. Transcriptional control of Dkk-1 was not due to changes in DNA methylation levels in the promoter region as methylation levels were no different when comparing AI and SCNT tissues. The decreased expression of Dkk-1 in SCNT cotyledons that are prone to abnormal placentation suggests a role in cotyledon formation but the mechanism and regulatory control is yet to be revealed. Key words: Dickkopf-1, DNA methylation, Placentation, Somatic cell nuclear transfer (SCNT) (J. Reprod. Dev. 55: [467][468][469][470][471][472][473][474] 2009) ovine placentation is a complex event involving a cascade of regulated gene expression where the attachment between maternal and fetal tissues begins between Days 20 to 30 of gestation and the placentome is not formed until around Day 50 of gestation [1][2][3]. Abnormal placentation is a major factor in failure of somatic cell nuclear transfer (SCNT) pregnancies in cattle [4][5][6] and can be used as a model to study events necessary for successful placentation. During a preliminary differential gene expression study comparing placental tissues obtained from Day 50 bovine artificially inseminated (AI) pregnancies with SCNT pregnancies we identified Dickkopf-1 (Dkk-1) as down-regulated in both fetal and maternal SCNT placentome tissue compared to AI tissue (unpublished data). Dkk-1 is a secreted glycoprotein that antagonizes the Wnt signaling pathway by binding to the Wnt coreceptors, lipoprotein receptor-related proteins (LRP) 5 and 6, and another transmembrane protein, Kremen, which then induces ...

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Section: Discussionmentioning

confidence: 81%

Dickkopf-1 Expression During Early Bovine Placentation and Its Down-regulation in Somatic Cell Nuclear Transfer (SCNT) Pregnancies

Ledgard

Lee

Couldrey

et al. 2009

Journal of Reproduction and Development

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“…The bTS cells established in our laboratory were similar in phenotype to mouse trophoblast stem cells and had the ability to differentiate into placenta trophoblast cells in vitro (Huang et al 2014). Ruminants have a distinct population of trophoblastic cells called binucleate cells (BNC) that account for approximately 20 % of the total trophoblast cell population (Wooding et al 1996). The BNCs are directly involved in modification of the uterine epithelium, beginning at implantation and continuing until term.…”

Section: Discussionmentioning

confidence: 99%

“…Coculture of bovine EECs and bovine trophoblast cells can be used to investigate the maturation of trophoblasts and the formation of binucleate cells. The binucleate cells (BNC) that account for approximately 20 % (15-20 %) of the total trophoblast cells are a distinct population of trophoblastic cells in ruminants (Wooding et al 1996). The BNCs plays a central role in forming the structures and secretions at the fetomaternal interface that are crucial in establishing and maintaining pregnancy in ruminant.…”

Section: Introductionmentioning

confidence: 99%

The bovine endometrial epithelial cells promote the differentiation of trophoblast stem-like cells to binucleate trophoblast cells

Hou

et al. 2016

Cytotechnology

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Endometrial epithelial cells (EECs) cultured in vitro are valuable tools for investigating embryo implantation and trophoblast differentiation. In this study, we have established the bovine EECs and trophoblast stem-like (TS) coculture system, and used it to investigate the binucleate cell formation of ungulates. The EECs was derived from the uterine horn ipsilateral to the corpus luteum by using collagenase I and deoxyribonuclease I, which exhibited typical epithelial morphology and were expressing bovine uterine epithelial marker such as IFNAR1, IFNAR2, Era, PGR, ESR1 and KRT18. The cells immunostained positively by epithelial and trophectoderm marker cytokeratin 18 (KRT18) and stromal marker vimentin antibodies, and the KRT18 positive cells reached 99 %. The EECs can be cultured for up to 20 passages in vitro with no significant morphology changes and uterine epithelial marker gene expression alteration. The bTS cells were established in a dual inhibitor system and exhibited typical trophoblast stem cell characteristics. When bTS cells were cultured with EECs, the bTS cells adhered to the EECs as adhering to feeder cells. Binucleate cells began appearing on day 4 of coculture and reached approximately 18.47 % of the differentiated cells. Quantitative real-time PCR or immunofluorescence analyses were performed on bTS cells cocultured at day 6 and day 12. The results showed that the expression level of KRT18 was down-regulated while the expression level of trophoblast differentiation marker MASH2, HAND1, GCM1 and CDX2 was upregulated in bTS cells. In conclusion, bovine EECs can be obtained from the uterine horn ipsilateral to the corpus luteum via treatment with collagenase I and deoxyribonuclease I, and the EECs-bTS cells coculture system presents an ideal tool for studying the differentiation of bTS cells to trophoblast binucleate cells.

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“…Evidence exists that protein expression in BCs is affected by anatomical location (Wooding et al 1996, Patel et al 2004b, and such differences in synthetic capacity appear to be more under maternal than foetal influence, since both cotyledonary and intercotyledonary tissues are exposed to a similar foetal environment (Wooding et al 1996). The presence of higher concentrations of bPL in IVP calves in the first hour after birth, along with higher concentrations in the allantoic fluid, suggests that a 'leakage' occurs from placental tissue to the foetal circulation, since no or negligible transfer of PL appears to occur from the maternal to the foetal circulation in sheep (Reddy & Watkins 1983).…”

Section: Discussionmentioning

confidence: 99%

Expression profile and protein levels of placental products as indirect measures of placental function in in vitro-derived bovine pregnancies

Bertolini¹,

Wallace²,

Anderson³

2006

Reproduction

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Bovine conceptus development and its association with placental proteins present in maternal, foetal and neonatal plasma and foetal (amniotic and allantoic) fluids were investigated in in vivo-and in vitro-produced (IVP) concepti and newborn calves. Females were superovulated to obtain control embryos, whereas IVP embryos were derived from established in vitro procedures. Pregnant animals were slaughtered on days 90 or 180 of gestation or allowed to develop to term for the assessment of physical traits. Foetal, maternal and neonatal blood and foetal fluids were collected for the determination of bovine placental lactogen (bPL) and bovine pregnancy-specific protein B (bPSPB) concentrations. Placental transcripts for bPL and bPSPB, determined by quantitative RT-PCR, were elevated in IVP placentomes. No major physical differences were observed between groups on day 90, but concentrations of bPL and bPSPB were higher in foetal plasma and allantoic fluid of IVP concepti in day 180 pregnancies, which were correlated with larger uterine and conceptus traits. Maternal concentrations of bPL in IVP pregnancies were lower than controls during the last 8 weeks of gestation, to become similar as parturition approached. Newborn IVP calves and foetal membranes were larger and displayed higher concentrations of plasma bPL than controls (10 and 60 min after birth). Our results indicated that differential patterns of secretion of bPL and bPSPB into the maternal and foetal systems occurred at distinct stages of gestation, and these were associated with altered conceptus development after in vitro embryo manipulations, indirectly demonstrating deviations in placental function in IVP pregnancies. Reproduction (2006) 131 163-173 IntroductionWith the onset of the trophoblast apposition to the endometrium during the process of bovine placenta formation and development, large granulated cells, the trophoblast binucleate cells (BCs), migrate from the trophectoderm to fuse with uterine epithelial cells (Wooding 1992), forming short-lived trinucleate cells. This phenomenon occurs throughout pregnancy in cattle, but the number and period of existence of trinucleate cells decline towards the end of gestation (Wooding 1992, Green et al. 2000. Binucleate cells comprise about 20% of the trophoblast cells and are responsible for hormones and bioactive products important for the regulation of foetal growth and development (Anthony et al. 1995, Green et al. 2000, Schlafer et al. 2000. The contents of the membranebounded secretory granules of BCs are released by exocytosis towards the maternal capillary bed, reaching the maternal blood system (Wooding 1992). Many proteins are produced by the BCs, including placental lactogen (PL) and a range of glycoproteins (Wooding 1992), such as pregnancy-specific protein B (PSPB) (Butler et al. 1982).PL lactogen is a member of the growth hormone (GH)/prolactin (PRL) gene family synthesized and stored in secretory granules of the trophoblast BCs (Byatt et al. 1992a, Wooding 1992, Gootwine 2004. Although ...

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Functional specialization in the ruminant placenta: Evidence for two populations of fetal binucleate cells of different selective synthetic capacity

Cited by 68 publications

References 18 publications

Dickkopf-1 Expression During Early Bovine Placentation and Its Down-regulation in Somatic Cell Nuclear Transfer (SCNT) Pregnancies

Dickkopf-1 Expression During Early Bovine Placentation and Its Down-regulation in Somatic Cell Nuclear Transfer (SCNT) Pregnancies

The bovine endometrial epithelial cells promote the differentiation of trophoblast stem-like cells to binucleate trophoblast cells

Expression profile and protein levels of placental products as indirect measures of placental function in in vitro-derived bovine pregnancies

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