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RESEARCH |
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100080, China
Correspondence should be addressed to Y-X Liu; Email: Liuyx{at}ioz.ac.cn
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Abstract |
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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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The STC-1 gene is widely expressed in various tissues. STC-1 is capable of promoting re-absorption of inorganic phosphate across renal and intestinal epithelia and reducing intestinal calcium transport (Wagner et al. 1997, Madsen et al. 1998). This hormone also has a possible role in maintaining the integrity of post-mitotic neurons (Zhang et al. 2000). The STC-1 gene has been found to be highly expressed in the ovary, in the androgen-producing thecal and interstitial cells (Deol et al. 2000, Paciga et al. 2002). The ovarian STC-1 is structurally unique and its expression is stimulated by human chorionic gonadotropin. This gene is also highly expressed during embryogenesis, particularly in the urogenital system, suggesting that STC-1 probably acts as a signaling molecule during embryo development (Varghese et al. 1998, Stasko & Wagner et al. 2001a). Recently, it has been observed that STC-1 is expressed uniquely in mouse mesometrial stromal cells and sequestered by decidualizing anti-mesometrial cells, indicating a possible role in decidualization and uterine remodeling (Stasko et al. 2001). The expression and regulation of STC-1 in rat uterus during early pregnancy is still undefined.
STC-2 also appears to be widely expressed in mammalian tissues, including kidney (Wagner et al. 1995), pancreas (Moore et al. 1999), skeletal muscle (Ishibashi et al. 1998), small intestine (Chang & Reddel 1998) and ovary (Honda et al. 1999). Compared with STC-1, however, the potential function of STC-2 is even less understood. There are no reports about its expression and possible role in the mammalian uterus. In the kidney, STC-2 was reported to have an inhibitory effect on the Na+/phosphate co-transporter activity while STC-1 is a stimulator of this transporter (Ishibashi et al. 1998). Honda et al.(1999) demonstrated that calcitriol, an active form of vitamin D3, increased STC-1 mRNA levels more than threefold, but decreased STC-2 message to a trace level, suggesting that STC-1 and STC-2 may be counteracting molecules, STC-1 being anti-hypercalcemic and STC-2 anti-hypocalcemic.
This information prompted us to consider whether the STC-1 and STC-2 genes are temporarily and spatially expressed and whether they counteract each other in the uterus during the processes of implantation and decidualization. To assess this possibility, we examined expression of both STC-1 and STC-2 in rat uterus during early pregnancy by RT-PCR, in situ hybridization and immunohistochemistry. Furthermore, we established various physiological states, such as pseudopregnancy, delayed implantation, artificial decidualization and embryo transfer to confirm it.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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To induce delayed implantation, pregnant rats were ovariectomized on D4 at 0830–0900 h and treated with progesterone (5 mg/rat, s.c.) to maintain the delayed implantation condition on D4–D7. On D8, a random half of the progesterone-primed delayed-implantation rats were additionally given estrodiol (250 ng/rat) to terminate the delayed implantation condition. The remaining animals only received progesterone injection. The rats were sacrificed for collection of the uteri 24 h after the last hormonal treatment. The implantation sites were identified by tail intravenous injection of Chicago blue solution. To confirm that the rats receiving progesterone only were in a state of delayed implantation, uterine flushings were collected and examined for the presence of hatched blastocysts.
Artificial decidualization
Mature rats were ovariectomized. Artificial decidualization was induced according to the procedures described by Kennedy & Ross (1997). The uteri were collected at 24, 48 and 72 h after injection of the oil.
Embryo transfer
Embryo transfer was performed as previously described by Ertzeid & Storeng (2001). On D4.5, pseudopregnant rats were anesthetized by intraperitoneal injection of ketamine. One lateral uterine horn was exposed via a lateral incision. The embryos to be transferred were collected from the pregnant donors on D4.5. A fine-tipped glass pipette was inserted into a hole made previously by insertion of a 23-gauge needle through the uterine wall at the oviductal end. The contralateral uterine horn served as the control. Thereafter, the uterine horns were returned to the abdominal cavity and the skin incision was sutured. On D6, the recipients were sacrificed 5 min after tail intravenous injection of trypan blue solution.
RT-PCR
Total RNA was extracted from rat uteri with Trizol reagent (Gibco BRL Life Technologies Inc., Rockville, MD, USA) according to the manufacturer’s instructions. The cDNA was synthesized from 1 µg total RNA using Superscript II reverse transcriptase (Gibco) and oligo dT. The reaction was carried out at 42 °C for 50 min and 70 °C for 15 min. For PCR analysis, the cDNA was amplified for 26 cycles (denaturing at 94 °C for 45 s, annealing at 55 °C for 45 s, and elongating at 72 °C for 45 s) using STC-1 and STC-2 primers respectively: STC-1 primers were 5'-TCTCTTGGGAGGTGCGTT-3' and 5'-GTCTTCCTTGCCATTCGG-3' (428–844 bp, Gene-bank accession number U62667
[GenBank]
), and the expected size of the amplified fragment was 417 bp. STC-2 primers were 5'-TTGTGAAATCCAGGGCTTA-3' and 5'-TAGGTGGTGGTCGGTGTC-3' (237–750 bp, Gene-bank accession number AB030707
[GenBank]
), with an expected product size of 514 bp. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) expression remains fairly constant in the rodent uterus and was amplified for 23 cycles as an internal control. The primers were 5'-ACCACAGTCCATGCCATCAC-3' and 5'-TCCAC-CACCCTGTTGCTGTA-3' (566–1017 bp, Genebank accession number M32599
[GenBank]
), with an expected size of 452 bp (Sidhu & Kimber 1999). PCR products were cloned into T-easy vector, screened by restriction analysis and confirmed by sequencing. To confirm the specificity of RT-PCR, three controls were included to test for contamination by genomic DNA: (1) RNA samples were directly amplified without reverse transcription; (2) reverse transcription was performed without adding reverse transcriptase, followed by PCR amplification; and (3) RNA samples were replaced with diethylpyrocarbonate–distilled H2O (DEPC–dH2O) in the RT-PCR.
In situ hybridization
In situ hybridization was performed as described previously. In brief, the uteri were cut into 4–6 mm pieces and flash frozen in liquid nitrogen. The frozen sections (8 µm) were mounted on 3-aminopropyltriethoxysilane (Sigma)-coated slides and fixed in 4% paraformaldehyde solution in PBS. The sections were treated in 0.2 N HCl for 10 min after two washes in PBS, digested with 0.1 µg/ml proteinase K at room temperature for 10–15 min, and incubated twice in 0.2% (w/v) glycine in PBS for 5 min. Postfixation was performed in 4% paraformaldehyde for 2 min. After acetylation in freshly prepared 0.25% (w/v) acetic anhydride in 0.1 M triethanolamine (pH 8.0) for 10 min, the sections were washed twice in 2 x SSC (0.3 M sodium chloride, 0.03 M sodium citrate) for 5 min, dehydrated in serial dilutions of ethanol, and air dried. Following the prehybridization in hybridization buffer (4 x SSC, 50% (v/v) formamide, 5% (w/v) dextran sulfate, 1 x Denhardt’s solution, 0.5 mg/ml denatured salmon sperm DNA, 0.25 mg/ml yeast tRNA) at 25 °C for 2–3 h, the sections were hybridized in hybridization buffer with 1–5 µg/ml DIG-labeled antisense or sense RNA probes at 55 °C for 16 h. After hybridization, the sections were washed in 4 x SSC at room temperature for 10 min and digested in 10 µg/ml RNase A (Boehringer Mannheim) in 0.01 M Tris–HCl and 0.5 M NaCl (pH 8.0) at 37 °C for 30 min. The sections were washed twice in 4 x SSC, 1 x SSC and 0.5 x SSC twice for 10 min at 42 °C. After non-specific binding was blocked in 0.5% (w/v) block mix (Boehringer Mannheim), the sections were incubated overnight in sheep anti-digoxigen (DIG) antibody conjugated to alkaline phosphatase at 4 °C (1:4000, Boehringer Mannheim). The signal was visualized with 5-bromo-4-chloro-3-indolyl phosphate and nitroblue tetrazolium. Endogenous alkaline phosphatase activity was inhibited with levamisole (Sigma).
Immunohistochemistry
Excised rat uteri were immediately fixed in 10% neutral Buffered Formalin solution and embedded in paraffin. Sections (5 µm) were cut, deparaffinized and rehydrated. Antigen retrieval was performed by incubating the sections in 0.01 M citrate buffer (pH 6.0) at 95 °C for 15 min and cooling naturally to room temperature for 20 min. Nonspecific binding was blocked in 10% (v/v) normal horse serum in PBS for 1 h. The sections were incubated with goat anti human STC-1 or STC-2 antibody in 10% (v/v) horse serum (1:100) for 12 h at 4 °C (SC-14346 and SC-14350 for STC-1 and STC-2 respectively, Santa Cruz Biotechnology Inc., Santa Cruz, CA, USA). The sections were then incubated with biotinylated secondary antibody followed by an avidin–alkaline phosphatase complex and Vector Red according to the manufacturer’s protocol (Vectastain ABC-AP kit, Vector Laboratories, Burlingame, CA, USA). Vector Red was visualized as a red color. Endogenous alkaline phosphatase activity was inhibited with levamisole (Sigma). As a negative control STC-1 or STC-2 primary antibody was replaced with normal goat IgG. The sections were counterstained with hematoxylin and mounted.
Microscopic assessment
Uterine samples from three individual rats from each group were analyzed. Experiments were repeated at least three times, and one representative section from at least three similar results is presented. The mounted sections were examined using a Nikon microscope.
Statistical analysis
Samples from three individual animals at each tissue collection time point were analyzed. Statistical analysis was performed using Statistical Package for Social Science (SPSS for Windows package release 10.0, SPSS Inc., Chicago, IL, USA). Statistical significance was determined by one-way ANOVA. Post-Hoc comparisons between treatment group means were made using Fisher’s protected least-significance-difference test. Differences were considered significant if P < 0.05. Values shown in all the figures were given as the mean ± S.E.M.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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) compared with those in the uteri on D5 of pregnancy, D6 of pseudopregnancy and delayed implantation. The densitometry analysis showed that the increase in both mRNA levels at the implantation site of pregnancy on D6, D8 and in the estrogen-activated delayed implantation uterus was very significant (P < 0.01), while the mRNA levels in the uteri on D5 of pregnancy, D6 of pseudo-pregnancy and delayed implantation were not significant (Fig. 1B). These data suggest that STC expression in the uterus is temporarily and spatially regulated.
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and data not shown). Significant STC-1 immunostaining was detected in the luminal epithelium on D1 and in both luminal and glandular epithelium on D2 of pregnancy (Fig. 3A, B). The immunostaining was markedly reduced thereafter. On D4 and D5, STC-1 immunostaining was moderate in the glandular epithelium and subluminal stroma, but it was weak in the luminal epithelium (Fig. 3C). While an elevated STC-1 signal was observed in the stromal cells near the lumen at the implantation site and embryo on D6 and D7 (Fig. 2C, F, Fig. 3D, E), no signal was observed at the implantation site on D6 of pregnancy when a DIG-labeled sense probe was used for hybridization (Fig. 2D). On D8, STC-1 signal in the primary decidual zone was still strong and gradually expanded to the secondary decidual zone (Fig. 2G). On D9, a high level of STC-1 was observed mainly in the secondary decidual zone (Fig. 2H), and high level of STC-1 immunostaining was observed in the whole decidua and the embryos on D8 and D9 of pregnancy (Fig. 3G and H). No immunostaining was detected when the goat anti-STC-1 was replaced with the normal goat IgG (data not shown).
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). No immunostaining was detected on D1 of pregnancy. From D2 on, however, a gradual increase in immunostaining in the glandular epithelium was observed, with maximal STC-2 immunostaining occurring on D5 (Fig. 5A, B). On D6 of pregnancy, when the blastocyst begins to implant, STC-2 mRNA levels were high and immunostaining was elevated in the stroma immediately surrounding the blastocyst (Fig. 4B, Fig. 5E). In the non-implantation site of the uterus, however, no mRNA was detected in the stroma, only a moderate immunostaining was observed in the glandular epithelium (Fig. 4C, Fig. 5G). From D7 to D9 of pregnancy, STC-2 mRNA was present in the decidual cells (Fig. 4E, G and H). Moderate levels of STC-2 immunostaining were strictly localized to the primary deciduas from D7 to D8 (Fig. 5H, I), while levels decreased in the whole deciduas on D9 (Fig. 5J). These data suggest that STC-1 and STC-2 may be induced by the process of blastocyst implantation, and that the molecules may be involved in the process of stromal cell decidualization.
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and 3F).
STC-2 mRNA was at a basal level during D1–D8 of pseudopregnancy (Fig. 4D). At the protein level, however, we observed a similar expression pattern as that in the uteri from D1 to D5 of early pregnancy (Fig. 5C, D). From D6 on, STC-2 immunostaining decreased gradually, reaching an undetectable level on D8 of pseudopregnancy (Fig. 5F). These results, combined with those obtained from early pregnancy, suggest that STC expression in the stromal cells in the recipient uterus was induced by the implanting blastocysts, while expression in the epithelial cells in the preimplantation uterus may be induced by non-embryonic factors, such as ovarian hormones.
STC expression during delayed implantation
STC-1 and STC-2 mRNAs were at a basal level in the uterus under delayed implantation conditions (Fig. 6A, 7A). After the delayed implantation was terminated by estrogen treatment, elevated STC-1 and STC-2 mRNA signals were induced in the stroma surrounding the blastocyst (Fig. 6C, 7C).
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, 7B). Once the delayed implantation condition was terminated by estrogen treatment, both STC-1 and STC-2 expression was strongly induced in the embryo and the sub-luminal stroma immediately surrounding the embryo (Fig. 6D, 7D). This result supports the hypothesis that the activated blastocysts specifically induce STC expression in the adjacent stromal cells.
STC expression during artificial decidualization
The initial attachment reaction between the uterine luminal epithelium and the blastocyst trophectoderm in rat occurs at 1200–1600 h on D5 of pregnancy and is rapidly followed by proliferation and differentiation of stromal cells into decidual cells (decidualization) (Psychoyos 1973). The decidual reaction can also be induced experimentally by an intraluminal injection of a small amount of oil into the uteri of pseudopregnant rats. To confirm whether STC expression in the decidualizing stromal cells is specifically induced after embryo implantation, we examined the expression of STC in artificial decidualization uteri. Basal levels of STC-1 and STC-2 mRNA were detected in the luminal epithelium in the untreated control horn (Fig. 6G, 7F), whereas STC-1 and STC-2 mRNA were high in the decidualized cells under artificial decidualization (Fig. 6E, 7E). A moderate level of STC-1 immunostaining was detected in the luminal epithelium of the untreated control horn (Fig. 6H). After decidualization was artificially induced, STC-1 immunostaining was increased in the decidualized cells (Fig. 6F).
We observed moderate STC-2 immunostaining in the decidualized stromal cells immediately under the lumen 24 hours after injection of the stimulated oil (Fig. 7G); the immunostaining was significant and expanded outward 48 hours later (Fig. 8H), while only a low level of STC-2 protein was detected in all decidual cells 72 h later (Fig. 7I). In the untreated control horn, immunostaining was detected in the glandular epithelium (Fig. 7J). These results are consistent with those observed in the uteri of the early pregnant decidualization, showing that STC expression is temporarily and spatially involved in the decidualization during the implantation process, and suggesting that STC-1 is involved in the entire decidualizaion process, while STC-2 may mainly participate in the primary decidualization.
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, both STC-1 and STC-2 mRNA and protein levels at the implantation site of the transplanted uteri were very similar to those in the uteri of early pregnancy (A, C, E, G), while in the non-transplanted control uteri, we observed the same expression pattern as that in the uteri of D5 early pregnancy (B, D, F, H). The data obtained from the embryo transfer model show a high similarity to the results from the early pregnancy and the delayed implantation models, confirming that STC expression in the receptive uterus was specifically induced by the implanting blastocysts. |
Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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It is interesting that a high level of STC-1 immunostaining was detected in the luminal epithelium at the implantation site on D6 of pregnancy. A similar expression pattern was also observed after the delayed implantation was terminated by estrogen treatment and embryo implantation was initiated. We also observed significant STC-1 immunostaining in the embryos of the pregnant uteri from D6 to D9, but no mRNA was detected in the post-implantation embryos. It is possible that STC-1 synthesized in the stromal cells at the implantation site may be transferred to or sequestered by luminal epithelium and embryos. A different localization of STC-1 mRNA and protein was noticed in the mouse uterus, where the STC-1 mRNA was uniquely expressed in the mesometrial stromal cells, while STC-1 protein was also localized in the decidualizing anti-mesometrial cells and the adjacent luminal epithelial cells (Stasko et al. 2001). The same mRNA-protein disparity in the adult mouse ovary was also reported by Deol et al.(2000).
Disparities between STC-1 mRNA expression and protein distribution were previously reported in other mammalian organs in addition to the uterus and ovary. During mouse urogenital development, a mesenchyme–epithelial signaling pathway was evident, whereby STC-1 mRNA was produced in the mesenchyme cells and the protein was much more evident in the adjacent epithelial cells (Stasko & Wagner et al. 2001a). During mouse skeletogenesis, the STC-1 gene was expressed in undifferentiated cells and targeted to cartilage cells in various stages of terminal differentiation (Stasko & Wagner et al. 2001b). It is evident that STC-1 plays a paracrine/ autocrine signaling role during these processes.
In our study, STC-1 mRNA levels and immunostaining were both evident in the decidualized cells on D7–D9 of pregnancy. Similarly, high levels of STC-1 mRNA and protein could be induced in decidualized cells under artificial decidualization. STC-1 expression in the decidual cells may suggest a role in decidualization. However, the mechanism of STC-1 action during this process is still unclear.
STC-2 mRNA was also highly expressed in the decidual cells on D7–D9 of pregnancy and in the artificially induced decidual cells. STC-2 protein expression was interesting, with only a moderate level of STC-2 immunostaining in the primary deciduas on D7–D8, and very low immunostaining in the whole deciduas on D9. Similarly, only moderate immunostaining was seen in the decidualized stromal cells immediately under the lumen 24 h after injection of the stimulating oil, the immunostaining was elevated and expanded outward 48 h later, while only a low level of STC-2 protein was detected in the whole decidual cell 72 h later. These data show that STC-2 may mainly participate in the process of primary decidualization. However, the mechanism by which STC-2 fulfills its function during decidualization remains to be discovered.
Intriguingly, we could only detect a basal level of STC-2 mRNA in the uterus during the preimplantation period, while a strong STC-2 protein signal was localized in the glandular epithelium before embryo implantation on D4–D5 of pregnancy. There are three possible explanations for the disparities. One possibility is that STC-2 immunostaining detected in the uterus was derived from the maternal serum, originating from organs other than the uterus that may play a role as an endocrine regulator of glandular proliferation/differentiation in the uterus. The localization pattern of STC-2 in the uterus was highly reminiscent of the ovarian STC-1 distribution during pregnancy and lactation and of their counterpart in fish, where the stanniocalcin appears to act in a classical endocrine fashion as a regulator of calcium and phosphate homeostasis (Paciga et al. 2002). Another possibility is that our in situ hybridization protocol might not be sufficiently sensitive to detect the mRNA signal. We consider this unlikely as we could detect the mRNA signal in the uterus once embryo implantation occurred, using the same experimental protocol. The third possibility is an upregulation mechanism of STC-2 protein by progesterone/estrogen at a translational level. No evidence is available in the literature, however, to support this hypothesis.
While the data from both ourselves and others (Deol et al. 2000, Stasko et al. 2001) show highly regulated STC-1 expression in the uterus and ovary, suggesting that STC-1 is involved in the regulation of uterine and ovarian function, the recently published STC-1 knockout paper presented us with unexpected results. The authors could not find any important change in fertility in STC-1 null mice, the histological examination of the uterus and ovary did not show any abnormalities compared with wild-type mice (Chang et al. 2005). The authors also ruled out the possibility of STC-2 compensating for the loss of STC-1, but checked STC-2 expression under normal status only. For figuring out the potential role of STC-1 in the uterus and the possibility of STC-1 function compensation by STC-2, the study should focus on the expression of STC-2 during different physiological conditions. It is also possible that compensation is fulfilled by other unknown candidates, the most efficient and accurate approach to figure this out would be to generate mice that are knockout both STC-1 and the candidate gene.
In summary, this is the first report to show expression and localization of both STC-1 and STC-2 in mammalian uteri under different physiological conditions. The high levels of STC expression at the implantation site and the decidual cells in rat uterus suggest that these hormones might be important for blastocyst implantation and uterine decidualization. STC-1 appears to be involved in the entire decidualization process, while STC-2 may participate mainly in the primary decidualization.
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Acknowledgements |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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The authors thank Dr Zengming Yang for his helpful suggestion on the experimental techniques and animal preparation. We also thank Dr Anne Grove for her valuable discussion and critical reading of this manuscript. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.
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Footnotes |
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Li-Juan Xiao and Jin-Xiang Yuan contributed equally to this work
Li-Juan Xiao is now at Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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