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RESEARCH |
Department of Animal Science, University of California, Davis, Davis, California 95616, USA and 1 Animal and Veterinary Science, University of Maine, Orono, Maine 04469, USA
Correspondence should be addressed to G B Anderson; Email: gbanderson{at}ucdavis.edu
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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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 its function and secretory control are not completely understood, in vivo and in vitro studies have suggested PL to have multiple somatogenic (GH-like) and lactogenic (PRL-like) biological effects, depending on the species, such as placental angiogenesis, maternal and foetal intermediate metabolism, mammary gland development and function, ovarian and placental steroidogenesis, growth rate and luteal function (Patel et al. 1996, Pedersen et al. 1998, Gregoraszczuk et al. 2000, Corbacho et al. 2002, Gertler & Djiane 2002, Gootwine 2004). Bovine (b) PL is more structurally similar to PRL than GH and is secreted into both the maternal and foetal systems (Gootwine 2004), with a decrease in foetal concentrations during the course of gestation and a peak in maternal plasma during the last trimester of pregnancy (Byatt et al. 1992a). It has been postulated that bPL recognizes homologous and heterologous somatogenic and lactogenic receptors, acting through components of the insulin-like growth factor system, which may modulate foetal growth (Byatt et al. 1992a, Anthony et al. 1995).
PSPB was first isolated from bovine placental tissues, as a product of the BCs of the trophoblastic ectoderm (Butler et al. 1982). Several isoforms of pregnancy-associated glycoproteins (PAG) from foetal cotyledons showing similarities with PSPB have been isolated (Zoli et al. 1991). Currently, PSPB is also known as PAG-1, being inactive members of the aspartic proteinase family (Xie et al. 1991, Lynch et al. 1992). Gene and cDNA sequencing have shown identical homology between PSPB and PAG-1, with both proteins differing only in glycosylation and sialic acid contents (Xie et al. 1991, 1995, Lynch et al. 1992). Concentrations of bPSPB in maternal plasma can be detected from early stages of gestation, during early placentation, to increase gradually throughout pregnancy and reach peak values immediately before parturition (Sasser et al. 1986, Kiracofe et al. 1993). Despite the unknown function and control of PSPB secretion, many potential biological functions have been suggested based on in vivo and in vitro effects, including prostaglandin release by the endometrium, implantation, immunotolerance of the conceptus as a tissue alograft and uterine remodelling after parturition, among others (Del Vecchio et al. 1990, 1995, 1996, Kiracofe et al. 1993, Austin et al. 1999, Tefera et al. 2001). Both PAG-1 and PSPB diagnostic assays have been developed for early plasma diagnosis of pregnancy in cattle and other ruminants (Sasser et al. 1986, Zoli et al. 1991, Green et al. 2000).
The amounts of BC products in maternal circulation appear to be associated with placental mass, foetal number and neonatal birth weight, and have been postulated to be an index for conceptus viability and pregnancy normalcy in cattle (Byatt et al. 1992a, Patel et al. 1995, 1996, 1997, Vasquez et al. 1995, Szenci et al. 1998, 2003, Tefera et al. 2001, Ravelich et al. 2004). Associations between abnormal placental and foetal development after in vitro embryo manipulations have been suggested to play a key role in the occurrence of high birth weights. Disturbances in placentation may at least partially affect the pattern of foetal growth (Hill et al. 2000, 2001, Bertolini et al. 2002a, Hashizume et al. 2002, Reik et al. 2003). Disruptions in BC function may compromise the viability and growth of the developing conceptus. Since significant spatial and temporal differences in the expression in the more than 20 identified bPAG cDNA isoforms appear to occur during bovine pregnancy (Green et al. 2000), distinct isoforms of the PAG-1 group may be more useful for the diagnosis of pregnancy and to predict deviations from normality. This study describes results using the same animals and samples as in previous reports (Bertolini et al. 2002a,b, 2004) to further investigate bovine foetal and placental development and their association with placental transcripts (bPL and bPAG-1) and plasma and foetal fluid protein concentrations (bPL and bPSPB) in in vivo-produced and in vitro-produced (IVP) concepti and newborn calves for use as potential biological markers for altered conceptus development after in vitro embryo manipulations.
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Materials and Methods |
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Embryo production, embryo transfer and pregnancy diagnosis
IVP and in vivo-produced (controls) Bos taurus embryos were generated according to our established procedures, as previously described (Bertolini et al. 2002a,b, 2004). We have adopted an IVP system known to induce, at a relatively high frequency, the appearance of symptoms of the Large Calf Syndrome (Behboodi et al. 1995, Bertolini et al. 2002a, 2004). Bovine cumulus–oocyte complexes from Angus–Hereford cross females were obtained either from a commercial source (Bomed Inc., Madison, WI, USA) or from a regional slaughterhouse. Donor females (Angus or Angus–Hereford crosses) were superovulated for the production of control embryos. Embryos were non-surgically recovered by uterine flushing on day 7 of development (artificial insemination = day 0). The same Angus sires were used for production of both control and IVP embryos. Blastocysts and expanded blastocysts from both embryo production systems (control and IVP) were non-surgically transferred to synchronous (±12 h) recipients on day 7 of development. Single embryos were transferred to recipients for the group of animals slaughtered on days 90 and 180, whereas one (in vivo singleton, in vitro singleton) or two (in vitro twin) embryos were transferred for the group of females allowed to carry pregnancies to term (Bertolini et al. 2002a, 2004). Pregnancy and foetal gender diagnoses were carried out by means of ultrasonography, per rectum, on days 27–30 and 58–60 of gestation respectively (Bertolini et al. 2002a, 2004).
Conceptus development and sample collection
Detailed morphometric, morphological and physiological data regarding foetal and placental development during pregnancy and after delivery for the group of recipients slaughtered on days 90 and 180 or allowed to carry pregnancies to term have been described previously (Bertolini et al. 2002a, 2004).
Days 90 and 180 of gestation
A group of pregnant females was slaughtered on days 90 or 180 of gestation (n = 4 in control and n = 5 IVP pregnancies for each day) for the collection of pregnant uteri and their respective foetuses and placental membranes. Pregnant females were allocated to each harvest day according to foetal gender and foetal viability after ultrasound examinations. In the control group (n = 8), animals carrying three females and one male were assigned to each harvest day (90 and 180) and, in the IVP group (n = 10), female recipients sustaining pregnancies with four females and one male were harvested on day 90, and recipients carrying three females and two males on day 180 of gestation. Foetal gender diagnoses performed on day 60 of pregnancy were all confirmed after harvest. Upon slaughter, reproductive tracts were excised and immediately weighed. Maternal blood samples were obtained at exsanguination. Following uterine dissection, foetal blood was collected by cardiopuncture, and total allantoic and amniotic fluid volumes were measured and sampled. Maternal and foetal blood, and amniotic and allantoic fluids were centrifuged, and plasma and fluids were frozen and stored at –80 °C pending analyses. Individual placentomes were weighed and measured (length and width) for estimation of the total gross surface area (SA). Placentomes were also classified into four categories by type according to gross morphological appearance, as follows: (A) engulfing mushroom-like, (B) sub-engulfing mushroom-like, (C) flattened, non-engulfing and (D) semi-convex placentomes (Fig. 1a
). Sample placentomes from the region immediately surrounding the foetuses were excised along their longitudinal axis, and pieces containing both maternal and foetal boundaries were snap-frozen in liquid nitrogen, stored at –80 °C and ultimately used for measurement of the relative transcription of genes of placental products (bPL and bPAG-1), as described below.
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bPL and pPSPB measurements in plasma and foetal fluids
Concentrations of bPL and bPSPB were determined by radioimmunoassay, in duplicates of maternal, foetal and neonatal plasma, and amniotic and allantoic fluids, according to established procedures by Wallace (1993) for bPL and Sasser et al.(1986) for bPSPB (BioTracking, Moscow, ID, USA). In this study, intra- and interassay coefficients of variation were 4.9% and 12.0% for bPL and 10.2% and 15.7% for bPSPB respectively.
Relative abundance of bPL and bPAG-1 transcripts in day-90 and -180 placentomes
A real-time TaqMan PCR (Applied Biosystems, Foster City, CA, USA) was optimized to quantify transcripts for bPL and bPAG-1 genes, following procedures described by Bertolini et al. (2002b, 2004). The analysis was performed at the Lucy Whittier Molecular Core Facility, School of Veterinary Medicine, University of California, Davis. Quantitative analyses of bovine cDNA from control and IVP day-90 and day-180 placentomes were performed in comparison with the endogenous control (glyceraldehyde-3-phosphate dehydrogenase; GAPDH), and were amplified in an automated laser-based fluorometer (7700 ABI PRISM Sequence Detection System; Applied Biosystems). Final quantification was done using the comparative CT method (Leutenegger et al. 2000). All samples were included in each assay, in single reactions, with one assay per transcript. Sequences of primers and probes for the transcripts are shown in Table 1.
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Results |
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Data regarding the comparison of physical traits between in vivo- and in vitro-derived concepti, newborn calves and term foetal membranes have been described previously (Bertolini et al. 2002a, 2004) and are summarized in Table 2. Placentomes were longer, wider and thinner (Fig. 1b
) in the IVP group (Bertolini et al. 2004), and distribution of placentome types was also different between groups (P < 0.05) on day 180 of pregnancy, with the occurrence of more uncommon types (C and D) in IVP pregnancies (Fig. 1c). The presence of such types, primarily type C, in controls was usually associated with small placentomes located in the nonfoetal horn, whereas these placentome types were randomly present in both uterine horns of IVP pregnancies in a wide size range. The difference in individual placentome size in the IVP group on day 90 of gestation, particularly in the foetal horn, was correlated with significantly higher (P < 0.05) concentrations of bPL and bPSPB in foetal plasma and allantoic fluid, and relative abundance of placentome transcripts for bPL and bPAG-1 in IVP concepti (Fig. 2a and b). On day 180, the relative abundance of placental transcripts for bPL and bPAG-1 (Fig. 2a and b) and uterine, foetal and placental physical component weights (Bertolini et al. 2004, Table 2) were larger in IVP pregnancies than in controls. Concentrations of bPSPB in the allantoic fluid of IVP pregnancies were 2.9-fold lower than controls (Fig. 2b) but, since day-180 IVP pregnancies had a 2- to 3-fold larger allantoic fluid volume than controls (Bertolini et al. 2004), total bPL and bPSPB in the allantois were higher and similar to controls respectively (Fig. 2c).
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. Temporally, concentrations of bPL were higher in the uterine compartments (foetal plasma and fluids) than in maternal plasma, apart from the experimental group (Pday < 0.05). In addition, maternal concentrations of bPL and bPSPB were higher on day 180 than on day 90 (Pday < 0.05), but lower in foetal plasma (bPL and bPSPB) and amniotic fluid (bPL). Positive correlations were observed between bPL and bPAG-1 transcripts (r = 0.824, P < 0.05), between bPL and bPSPB concentrations in the same fluid type (maternal plasma, r = 0.715, foetal plasma, r = 0.635, amniotic fluid, r = 0.505, P < 0.05, except in allantoic fluid), and between maternal concentrations of bPL and bPSPB (r > 0.850, P < 0.05), and with glucose and fructose accumulations (r > 0.650, P < 0.05) in the uterine compartments (data not shown, Bertolini et al. 2004). Positive correlations were observed also between conceptus component weights, substrate (glucose and fructose, data not shown) accumulations and bPAG-1 transcripts (r > 0.600, P < 0.05).
Plasma concentrations of bPL throughout gestation in pregnant females carrying in vivo singleton, in vitro singleton and in vitro twin concepti are illustrated in Fig. 3. Three distinct phases can be visualized in the weeks preceding parturition, based on the variation in bPL concentrations among groups (Fig. 3). In phase I (weeks 39 and 24 prepartum), no differences in concentrations of maternal plasma bPL were observed between groups. Then, in phase II (week 23 to week 8–9 prepartum), concentrations of maternal bPL were significantly higher in the in vitro twin group (P < 0.05). In phase III (week 8–9 to week 1 prepartum), maternal concentrations in the in vitro singleton group were lower (P < 0.05), but similar to controls and the in vitro twin group as parturition approached. At delivery, concentrations of maternal plasma bPL were significantly different between groups (in vivo singletons < in vitro singletons < in vitro twins, P < 0.05), to become similar 24 h after parturition.
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, for a steady increase in plasma concentrations from early to late pregnancy, with a decline following parturition. The in vitro singleton group had lower bPSPB concentrations than controls and the in vitro twin group in the week and the day immediately preceding and following parturition respectively (P < 0.05), but no other significant differences were observed between groups at any further stage of gestation examined.
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). Plasma concentrations of bPSPB tended to be higher (P < 0.08) and became significantly higher (P < 0.05) in the in vitro singleton group 60 min and 24 h after birth respectively (Fig. 5b). Concentrations of bPL and bPSPB in the first 60 min postpartum were positively correlated with neonatal and foetal membrane physical traits (r > 0.800, P < 0.05), and correlated with neonatal plasma fructose concentrations (data not shown, Bertolini et al. 2004).
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Discussion |
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In this study, placental and foetal membrane weight and placental and cotyledonary SAs were greater in IVP pregnancies, and both mass and SAs increased as a function of the increase in placentome length and width, but placentomes were thinner at both days 90 and 180 of gestation. Changes in placental morphology and deviations in the morphological distribution of the placentome type (fewer types A and B and increased unusual C and D types) were readily detectable in the first and second trimester of gestation in IVP pregnancies (Fig. 1). Such variations in placentome types may reflect anatomical, histological and functional differences in development, and such changes may ultimately influence placental transport efficiency, function, metabolism and synthetic capacity. Under physiological conditions, the placenta grows faster than the foetus in early pregnancy but slower after mid-gestation, when foetal weight surpasses that of the placenta (Eley et al. 1978, Prior & Laster 1979, Reynolds et al. 1990). Morphologically, the bovine placenta is considered fully developed at mid- to late gestation, but foetal villous trees continue to develop (branching pattern) and rearrange (spatial relationship between endothelium and trophoblast) in placentomes until near term, increasing the villous SA, which will also accommodate foetal demands for growth towards the end of gestation (Leiser et al. 1997). However, the placental tissue holds a great plastic capacity in facing unusual, adverse circumstances. Maternal dietary restriction or hypoxia in early gestation in cattle and sheep can initially impair such a standard pattern of placental growth (Penninga & Longo 1998, Perry et al. 1999, Wallace et al. 1999, Symonds et al. 2001) but, once dietary intake is restored to normal, a placental and foetal growth compensatory enhancement is observed. A coincidental aspect of these findings with our studies is that IVP concepti were significantly smaller during the period of placentation to the early foetal stage (up to day 58 of gestation), which appeared to have preceded a subsequent compensatory growth initiated with the placental tissue and followed by the foetus (Bertolini et al. 2002a). A hormonal effect of PSPB has been demonstrated in inducing the in vitro release of an 
chemokine (granulocyte chemotactic protein-2) by the endometrium, which may be relevant for implantation and placental angiogenesis (Austin et al. 1999). Bovine placental PAG-1 and foetal plasma PSPB were elevated in the IVP group at a time at which placental compensatory growth was already detectable (day 90).
The amounts of placental products in maternal circulation appear to be associated with placental and foetal masses, including foetal number and neonatal birth weight, and with pregnancy normalcy (Byatt et al. 1992a, Patel et al. 1995, 1997, Vasquez et al. 1995, Tefera et al. 2001, Gootwine 2004). In this study, concentrations of maternal and foetal plasma bPL followed similar trends reported by Hossner et al.(1997), Holland et al.(1997) and Patel et al.(1996), but concentrations of bPL and bPSPB in foetal plasma were correlated with conceptus physical traits and with one another in plasma and fluids. Anthony et al.(1995) suggested that a relationship exists between ovine PL gene expression and the rate of ovine PL appearance in foetal circulation, an observation that appears to be valid for our findings with both bPL and bPSPB. Increased bPL and bPSPB relative mRNA abundances in day-90 and day-180 placentomes and concentrations in the foetal plasma and allantoic fluid on day 90, along with accumulations of glucose and fructose in foetal plasma and associated fluids (Bertolini et al. 2004), were associated with an increase in prenanatal growth and foetal number in IVP concepti. As placentomes from IVP pregnancies were distinct from controls in terms of morphology, mass and surface area, the pattern of secretion of BC products may have been affected and explain some of the distinct patterns seen in IVP pregnancies.
The elevation in bPL in the third trimester of pregnancy coincides with the period of faster foetal growth and mammogenesis (Patel et al. 1996). In fact, newborn IVP calves coincidentally displayed higher birth weights and plasma bPL and fructose concentrations immediately after birth (Bertolini et al. 2002a, 2004). Conversely, maternal concentrations of bPL during phase III of pregnancy (Fig. 3) in the in vitro singleton group were lower than in vitro twin and in vivo singleton groups and, at parturition, maternal bPL concentrations in in vivo-produced pregnancies fell earlier than in those that were in vitro derived (Fig. 3). Interestingly, Miles et al.(2004) reported a reduction in foetal villi and BC volume densities in day-222 IVF-derived placentomes, which coincides with the period of decrease in maternal bPL levels in females carrying IVP singleton foetuses in this study.
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). Such findings corroborate the concept that the pattern of secretion of bPL in the foetal circulation may be relevant for foetal growth (Byatt et al. 1992a) and disturbances in placental formation may lead to such differential pattern of bPL secretion between the maternal and uterine compartments (Ravelich et al. 2004).
In addition to placental mass, parity and nutrition also appear to modulate the secretion of bPL. However, Patel et al.(1996) did not find distinctions in maternal bPL concentrations between singleton- and twin-bearing pregnancies, which the authors explained as a reduced placental mass per foetus in twin-bearing pregnancies. For singleton-bearing pregnancies, a relationship exists between placental and neonatal birth weights and maternal bPL concentrations, which could be used as a marker for conceptus development, viability and predicting abnormal birth weights (Patel et al. 1996). The half-life for the recombinant bPL has been reported to be 7.5 min (Byatt et al. 1992b), which is shorter than for GH or PRL but, as native bPL is heavily glycosylated (Byatt et al. 1992a), a half-life similar to GH and PRL (20 to 30 min) is expected, which is visible in plasma of newborn calves in the first 60 min following birth (Fig. 5a). Conversely, as bPSPB has a rather long half-life, with its plasma levels still detectable 3 months or more after parturition (Sasser et al. 1986, Kiracofe et al. 1993), neonatal plasma concentrations remained elevated throughout the period under scrutiny (24 h) following parturition (Fig. 5b). However, differences in plasma clearance perhaps highlight bPL as a more dependable marker for pregnancy normalcy than bPSPB.
Many of the changes in placental development and function in the IVP group in this study were associated with the accelerated pattern of foetal growth, the delivery of larger calves, and the appearance of aberrant foetal membranes at term, and an increase in substrate uptake and protein synthetic capacity in IVP pregnancies (Bertolini et al. 2002a, 2004). Concentrations of bPL and bPSPB in foetal plasma were correlated with physical traits and with one another in foetal plasma and associated fluids irrespective of the experimental groups. Differential patterns of secretion of bPL and bPSPB into the maternal and foetal systems occurred at distinct stages of gestation, which were associated with altered conceptus development after in vitro embryo manipulations, indirectly demonstrating differences in placental function in IVP pregnancies. However, bPSPB/bPL prenatal measurements in foetal plasma and fluids were useful indicators of abnormal growth and development, but such invasive measurements lack a practical application.
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Acknowledgements |
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Footnotes |
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References |
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