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RESEARCH |
Hokkaido Animal Research Center, Shintoku, Hokkaido 081-0038, Japan1 Department of Animal Science, Faculty of Agriculture, Iwate University, Morioka, Iwate 020-8550, Japan2 National Livestock Breeding Center Tokachi Station, Otofuke, Hokkaido 080-0572, Japan3 Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan4 Reproductive Biology Research Unit, Division of Animal Science, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-0901, Japan5 Hokkaido Konsen Agricultural Experiment Station, Nakashibetsu, Hokkaido 086-1135, Japan
Correspondence should be addressed to H Hirayama; Email: h.hirayama{at}agri.pref.hokkaido.jp
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Abstract |
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Introduction |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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Placental estrogens, estrone (E1) and estradiol-17β (E2), have been suggested to play important roles in the parturition process (Wood 1999). Uterine contraction is essential for the process of parturition, and placental estrogens influence the activity of the uterine myometrium (Wathes & Porter 1982). Also, placental estrogens may dilate the cervix that allows passage of the fetus through the birth canal (Breeveld-Dwarkasing et al. 2003). Estrogens are synthesized by aromatase (CYP19), which converts androgens into estrogens in fetal cotyledonary tissue (Schuler et al. 2006), and show a dramatic increase in maternal plasma during the pre-partum period (Takenouchi et al. 2004). The activity of estrogen is regulated by sulfoconjugation that inhibits the binding of steroids to their nuclear receptors. Estrone sulfate (E1S) is an inactive form catalyzed by estrogen sulfotransferase (SULT1E1), the activity of which is detected mainly in fetal cotyledonary tissue (Hoffmann et al. 2001). Conversely, sulfoconjugated estrogens may also be precursors of the production of free estrogens, depending on placental estrogen sulfatase (STS) activity (Rossier & Pierrepoint 1974).
Cortisol, a well-known trigger initiating the parturition process, induces an increase in the synthesis of estrogens in the placenta (Wood 1999). A previous report suggested that the prenatal cortisol rise in clone fetuses was insufficient and therefore parturition was not spontaneous (Matsuzaki & Shiga 2002). By contrast, another study demonstrated a normal cortisol response to adrenocorticotropic hormone (ACTH) in neonatal clone calves, implying that the calves had a mature cortisol secretion system (Chavatte-Palmer et al. 2002).
Previously, several investigators suggested morphological and functional abnormalities of the placenta in clone fetuses in various gestational stages (Hill et al. 2001, Hashizume et al. 2002, Constant et al. 2006); however, the role of the placenta in the final process of pregnancy, namely placental steroidgenesis and regulation of hormonal activity, is not fully understood. Therefore, analyses of placental events on the parturition process may help to overcome problems in the pre-partum period. The aim of this study was to elucidate the factors causing a poor sign of parturition and prolonged gestation in clone pregnancies. We assessed maternal plasma E1, E2, E1S, and progesterone (P4) concentrations during the pre-partum period and plasma cortisol concentration in newborn calves. Furthermore, we analyzed mRNA expression levels and localization of estrogen-metabolizing genes, SULT1E1, STS, and CYP19, in the placenta at parturition.
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Results |
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Maternal plasma hormone concentrations
Hormone concentrations were measured in 13, 8, and 4 cows for VC, CC, and Control respectively. The data are shown in Fig. 1.
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Control recipients exhibited a marked increase in plasma E2 concentration prior to the induction of parturition. Plasma E2 concentration of VC recipients increased gradually, but clone pregnancies showed lower concentrations than Control recipients in the pre-parturition period.
Plasma E1S concentration in clone pregnancies increased gradually from pre-initiation of the induction of parturition whereas plasma E1S concentration in Control recipients only increased at term. As a result, plasma E1S concentration in clone pregnancies tended to be higher than those in Control recipients during the pre-parturition period.
E1/E1S ratio in Control recipients showed progressive increase from day 271 of pregnancy to just before prostaglandin (PG)F2
treatment and then declined at term. Increase in the E1/E1S ratio in VC recipients was modest in comparison and CC recipients did not show any increase in the ratio throughout the same period.
Plasma P4 concentration decreased gradually from initiation of the induction of parturition and there was no significant difference in VC, CC, and Control recipients at any time point.
Plasma cortisol concentrations in calves
Plasma cortisol concentrations in calves were measured in 17 VC, 10 CC, and 9 Control. Plasma cortisol concentrations in VC (104.4±23.1 ng/ml) and Control (93.4±15.0 ng/ml) were similar and tended to be higher than for CC (60.1±19.1 ng/ml; P>0.05).
Messenger RNA abundances of SULT1E1, STS, and CYP19 in placentomes at parturition
Messenger RNA abundances were analyzed in 7, 10, and 4 samples in the cotyledonary villi (COT) and 5, 9, and 4 samples in the caruncle areas (CAR) for VC, CC, and Control respectively.
Messenger RNA abundance for SULT1E1 did not differ significantly between COT and CAR (Fig. 2A). Placental mRNA abundances of SULT1E1 were significantly higher in VC and CC than in Control.
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Messenger RNA abundance for CYP19 was significantly higher in COT than in CAR (Fig. 2C). There was no difference between VC, CC, and Control placentomes.
Correlations between placental mRNA abundances and estrogen concentrations in clone pregnancies
As shown in Table 1, mRNA abundance of SULT1E1 in COT was negatively correlated with maternal plasma E1 concentration (P<0.05) and positively correlated with maternal plasma E1S concentration (P<0.05). Positive correlations between mRNA abundances of STS and CYP19 in CAR and maternal plasma E2 concentration were also statistically significant.
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There were no significant differences among the numbers of BNC in VC (18.8±1.4/0.1 mm2), CC (18.6±1.7/0.1 mm2), and Control (18.9±1.8/0.1 mm2).
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Discussion |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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The rise of plasma E1 and E2 concentrations in cows carrying control fetuses started before the induction of parturition. By contrast, plasma estrogen concentration in cows carrying clone fetuses was low at that time, and the increase during the last few days of pregnancy was also subtle. Cows that delivered calves via cesarean section showed particularly low levels of plasma estrogens. Therefore, our results suggested that the estrogen activity necessary for the parturition process was insufficient in clone pregnancies, in spite of an adequate gestation length and the induction of parturition. In addition, plasma E1S concentration in clone pregnancies tended to be higher during that period. Maternal E1S concentration is usually 10- to 15-fold higher than that of E1 during most of the gestation period; however, in cows carrying clone fetuses, plasma E1S concentrations were 
20- to 60-fold higher than those of E1 at parturition, so the E1/E1S ratio was very low during late gestation. Therefore, the apparent lack of preparation for parturition in cows carrying clone fetuses could be explained by insufficient estrogen synthesis and/or increased metabolism of active estrogens to inactive estrogens.
Clone pregnancies exhibited high placental SULT1E1 expression compared with control pregnancies, and it seemed that sulfoconjugation activity in clone placenta was facilitated at parturition. Indeed, SULT1E1 mRNA abundance in COT of clone pregnancies correlated negatively and positively with maternal plasma E1 and E1S concentrations respectively. Although we have not obtained a dataset of mRNA abundance associated with plasma estrogen concentration in control pregnancies, the present results suggested that abundantly expressed SULT1E1 might inhibit the pre-partum rise of unconjugated estrogens. Previous studies clearly showed that SULT1E1 located in BNC by immunohistochemistry (Brown et al. 1987) and COT had high sulfoconjugation activity compared with CAR (Hoffmann et al. 2001). In this study, because in situ hybridization signals to SULT1E1 were localized in BNC, RT-PCR amplicons detected in CAR might be due to contamination from COT when tissues were separated manually.
The placental BNC population in clone pregnancies during early to mid-gestation (days 30–150) has been analyzed by several investigators, with results ranging from fewer (Hashizume et al. 2002, Arnold et al. 2006) or similar (Hoffert et al. 2005) to more (Ravelich et al. 2004) compared with pregnancies with in vivo- and in vitro-derived embryos. The present study showed that the BNC population at full term was similar in clone and control pregnancies, so it can be surmised that increased SULT1E1 mRNA abundance in clone placenta was due to increased transcription of the gene and/or increased proportion of SULT1E1 producing BNC.
Although P4 and androgen appear to induce the transcription of SULT1E1 in human endometrium and Leydig cells respectively (Falany & Falany 1996, Qian & Song 1999), the transcriptional control of SULT1E1 in BNC is still unclear. On the other hand, it is known that the concentration of maternal sulfoconjugated estrogen, E1S, positively correlates with the birth weight of calves and the weight of COT (Echternkamp 1993, Zhang et al. 1999). In addition, E1, E2, and E1S concentrations in twin-bearing cows are significantly higher than those in singleton cows during the third trimester (Takahashi et al. 1997, Patel et al. 1999). In these cases, sulfoconjugation may be facilitated in association with the increase in placental estrogen synthesis. Morphological and histological studies have shown enlarged placentomes and overgrowth of COT in clone pregnancies (Lee et al. 2004, Constant et al. 2006), and the birth weight of clone calves in this study was significantly heavier. Also in this study, there was a positive correlation between E1S concentration and birth weight in the pooled dataset comprising VC, CC, and Control pregnancies (r=0.43, P=0.032). However, while clone pregnancies had elevated maternal E1S concentration, E1 and E2 were actually decreased relative to Control pregnancies. Therefore, it appears that in clone pregnancies placental sulfoconjugation by SULT1E1 is not adequately regulated.
Placental expression levels of STS and CYP19 mRNA did not differ between clone and control pregnancies. At the time of parturition of clone fetuses, mRNA abundances of these genes in placentomes were positively correlated with maternal E2 concentrations. Therefore, it appears that STS and CYP19 contribute to the progress of parturition by desulfation and de novo synthesis of estrogen respectively. Data by real-time RT-PCR showing high STS expression in CAR and high CYP19 expression in COT agreed with the previous reports on normal pregnancies (Tsumagari et al. 1993, Hoffmann et al. 2001). Also, the localization of positive cells for STS and CYP19 is consistent with earlier reports (Schuler et al. 2006, Greven et al. 2007). These results suggest that excess sulfoconjugation of estrogens is a possible cause for a poor sign of parturition and prolonged gestation in clone pregnancies, rather than insufficient supply of active estrogens.
The induction of parturition in pregnant cows using dexamethasone and PGF2 has been performed in many studies on somatic clone cattle (Hill et al. 1999, 2001, Matsuzaki & Shiga 2002, Pace et al. 2002). This is mainly conducted to avoid dystocia due to LOS and prolonged gestation. Dexamethasone is a synthetic glucocorticoid and acts as cortisol, which is secreted from the fetal adrenal cortex. It is known that cortisol enhances estrogen synthesis in the placenta and plays a major role in the initiation of parturition (Wood 1999). Matsuzaki & Shiga (2002) reported that the plasma concentration of cortisol in neonatal clone calves was significantly lower than that in control calves, which were produced by artificial insemination and in vitro fertilization. By contrast, we found similar cortisol concentrations between vaginally delivered clone and control calves. Although the reason for the contradictory results between the two studies is unknown, the present study suggested that clone calves had the ability to synthesize cortisol at parturition. In support of this notion, the results of an ACTH stimulation test showed that the adrenocortical response of neonatal clone calves was normal (Chavatte-Palmer et al. 2002). In this study, cesarean section delivered clone calves, which should not be stressed in the birth canal, had slightly lower cortisol concentration. For these calves, there is also a possibility that preparation for parturition was poorer, resulting in having to be delivered by cesarean section and this may be reflected in the lower cortisol concentration in the calves. Furthermore, since P4 concentration decreased similarly following PGF2 treatment in cows carrying clone and control fetuses, luteolysis progressed normally regardless of the origin of the fetus. Thus, we could not find any abnormality of the neonatal cortisol level and luteolysis, which contribute toward fetal maturation and signal readiness for birth. However, to our knowledge, there has been no report demonstrating the normality of cortisol synthesis in prenatal clone fetuses. Further study to confirm the secretion level of cortisol in clone fetuses is necessary.
In summary, this report revealed that maternal estrogen concentrations in clone pregnancies did not increase sufficiently in the pre-partum period. Due to elevated placental SULT1E1 expression level, it is suggested that excess placental sulfoconjugation is a factor inhibiting the pre-partum rise of active estrogen and causes a poor sign of parturition in clone pregnancies.
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Materials and Methods |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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The induction of parturition in cows was achieved with 20 mg i.m. dexamethasone (Denka Pharmaceutical Co., Kawasaki, Japan) at days 276–288 of pregnancy, followed by PGF2 (0.75–1 mg i.m. cloprostenol (Resipron-C, Aska Pharmaceutical Co., Ltd, Tokyo, Japan) or 25 mg i.m. tromethamine dinoprost (Pronalgon-F injection, Pharmacia)) and 20 mg i.m. estriol (Holin, Teikoku Zoki Co., Tokyo, Japan) 24 h later. The calves were delivered 2 or 3 days after the administration of dexamethasone. Some control calves were delivered by cesarean section, after the induction of parturition. The decision whether to allow vaginal delivery or to perform cesarean section was based on subjective comparison of fetal size, maternal pelvic diameter, and soft birth canal diameter. Average days of gestation when induction of parturition was initiated were day 282 (range days 277–288), day 283 (days 276–285), and day 283 (days 280–288) for VC, CC, and Control respectively.
Venous blood samples of cows were taken at days 257 and 271 of pregnancy and just before dexamethasone treatment, PGF2 treatment, and parturition. Venous blood samples of calves were taken just after parturition. Plasma was harvested by centrifugation and stored at –20 °C until analyses.
Placentomal tissues were collected manually, immediately after vaginal delivery and cesarean section, through either the birth canal or incision site of the uterus respectively. Placentomes were fixed in 10% formalin neutral buffer solution (pH 7.4) and then embedded in paraffin wax and stored at 4 °C prior to in situ hybridization and immunohistochemistry. Additional placentomes were separated into two portions manually, COT and CAR, and the collected samples were stored at –80 °C prior to RNA extraction.
The number of animals and samples used for each assay is given in the Results.
Hormone assays
Hormone assays were carried out in duplicate by double-antibody enzyme immunoassay (EIA), as described previously (Miyamoto et al. 1992).
E1 concentration was measured by the EIA technique, as described by Acosta et al. (2002). Dilutions of anti-estrone-3-glucuronide-BSA IgG (anti-E1; Cosmo Bio Co., Ltd, Tokyo, Japan) and estrone-3-carboxymethyl ether-horseradish peroxidase (CME-HRP) (Cosmo Bio) were 150 000 and 70 000 respectively. Cross-reactivity of anti-E1 with E1, E1-glucuronide, E1S, and E2 were 100, 17, 25, and 1% respectively. The standard curve for E1 ranged from 0.75 to 1000 pg/ml. The ED50 value of the assay was 423 pg/ml. The averages of intra- and inter-assay coefficients of variation (CVs) were 8.0 and 12.2% respectively.
Plasma E2, P4, and cortisol were determined after extraction by diethyl ether. The EIA for E2, P4, and cortisol was performed as described previously (Acosta et al. 1998, 2002). The standard curve ranged from 2 to 2000 pg/ml for E2, 0.05 to 50 ng/ml for P4, and 0.1 to 100 ng/ml for cortisol. ED50 values of the assay for E2, P4, and cortisol were 40 pg/ml, 1.8 ng/ml, and 6.4 ng/ml respectively. The average of inter- and intra-assay CVs for E2, P4, and cortisol were 7.1 and 9.8%, 6.2 and 9.3%, and 8.9 and 11.1% respectively.
E1S concentration was measured by the EIA technique described by Isobe & Nakao (2002) with minor modifications. Anti-estrone-3-sulfate-6-(O-carboxymethyl) oxime (CMO)-BSA IgG (anti-E1S) and estrone-3-sulfate-6-CMO-HRP (E1S-HRP) were generously supplied by Kambegawa Institute (Tokyo, Japan). Cross-reactivities of anti-E1S with E1S, E1, estrone-3-glucuronide, estradiol-3-sulfate, and estradiol-3-glucuronide were 100, 8, 4, 0.4, and 0.2% respectively. E1S standards were diluted with assay buffer supplemented with 5% plasma from nonpregnant cows. Fifteen microliters of E1S standard (0.06–1000 ng/ml) or plasma samples were added to each well coated with anti-rabbit 
-globulin antiserum. In addition, 100 µl anti-E1S (x2 000 000) were distributed into all wells and then incubated for 16 h at 4 °C. After decanting the plates, 100 µl E1S-HRP (x800 000) was distributed into all wells and then incubated for 2 h at 4 °C. Finally, colorimetric treatment was carried out. The ED50 value of the assay was 32.0 ng/ml. Intra- and inter-assay CVs were 10.7 and 15.2% respectively.
Reverse transcription and real-time PCR
Total RNA was individually isolated from COT and CAR using ISOGEN (NipponGene, Toyama, Japan) and reverse transcribed using QuantiTect Reverse Transcription Kit (Qiagen Inc.) according to the manufacturer's instructions.
Real-time PCR was performed (run in duplicate) using QuantiTect SYBR Green PCR Kit (Qiagen) and Chromo 4 Real-time PCR system (Bio-Rad Laboratories, Inc). The primers for SULT1E1, STS, CYP19, and ACTB and annealing temperatures are listed in Table 2. The thermal cycling conditions included the activation step of HotStarTaq DNA polymerase at 95 °C for 15 min, followed by 45 cycles of denaturation at 94 °C for 15 s; annealing of primers at different temperatures (Table 2) for 30 s; and elongation at 72 °C for 30 s. To quantify the mRNA abundances, standard curves for each gene were generated by serial dilution of a known quantity of purified RT-PCR products. The relative difference in the initial amount of each mRNA species was determined by comparing the Ct values. We confirmed the melting curve for detecting the SYBR Green-based objective amplicon because SYBR Green also detects double-stranded DNA, including primer dimers, contaminating DNA and PCR products from misannealed primers. The expression ratio of each gene to ACTB mRNA was calculated for adjustment of the amount of RNA used the RT-PCR.
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In situ hybridization
Digoxigenin (DIG)-labeled anti-sense and sense cRNA for SULT1E1 and STS were prepared using DIG RNA Labeling Kit (Roche Diagnostics GmbH) including T7 RNA polymerase. T3 RNA polymerase (Roche) was purchased separately. Briefly, RT-PCR was performed using a HotStarTaq Master Mix Kit (Qiagen) and specific primers used for the above-mentioned real-time PCR, but forward and reverse primers were added from the T3 and T7 promoter sequence to the 5'-end respectively. A total of 200 ng PCR products were used as templates for synthesizing a hybridization probe. Paraffin-embedded placentomes were sectioned into 7 µm thick sections. In situ hybridization was performed using an automated Ventana HX System Discovery with a RiboMapKit, an AmpMapKit (Tyramide Signal Amplification system), and a BlueMapKit (BCIP/NBT stain system; Ventana, Tucson, AZ, USA). The sections were hybridized with DIG-labeled probes in Ribohybe (Ventana) hybridization solution at various temperatures (61–65 °C) for 6 h, then washed for 3x6 min in RiboWash (Ventana) at 65 °C, and fixed in RiboFix (Ventana) at 37 °C for 10 min. SULT1E1 and STS hybridization signals were detected using a rabbit polyclonal anti-digoxigenin HRP conjugate (Dako Cytomation, Carpinteria, CA, USA; Table 2).
Immunohistochemistry
Paraffin-embedded placentomes were sectioned into 7 µm thick sections. Immunohistochemistry was performed using an automated Ventana HX System Discovery with a DAB Map kit (Ventana). Briefly, the sections were incubated with an anti-aromatase polyclonal antibody (#3599-100, Biovision Research Products, Mountain View, CA, USA) diluted 1:20 in Discovery Ab diluent (Ventana) for 30 min at room temperature. Signals were detected using an anti-rabbit IgG polyclonal antibody biotin conjugate (Sigma).
Number of BNC
Five micrometer sections of paraffin-embedded placentomes were prepared and stained with hematoxylin–eosin. Three fields (0.109 mm2/field) of view of each placentome section were recorded under the light microscope with a digital photo system. Basal secondary villi or tertiary villi (Schuler et al. 2006) were examined for evaluation of BNC. Average number of BNC in three fields was calculated as a representative value and corrected to per 0.1 mm2.
Statistical analysis
All results are presented as the mean±S.E.M. Statistical analysis was performed using the Kruskal–Wallis test and Scheffe's test for post hoc analysis except that results of real-time PCR were analyzed using two-way ANOVA and Scheffe's test. Significance of the correlation coefficient between hormonal concentrations and mRNA abundances was assessed by regression analysis.
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Declaration of interest |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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Funding |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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Received 8 April 2008
First decision 15 July 2008
Revised manuscript received 14 May 2008
Accepted 28 July 2008
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References |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingReferences |
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