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BOR - Papers in Press, published online ahead of print December 11, 2002.
Biol Reprod 2002, 10.1095/biolreprod.102.009761
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BIOLOGY OF REPRODUCTION 68, 1787–1792 (2003)
DOI: 10.1095/biolreprod.102.009761
© 2003 by the Society for the Study of Reproduction, Inc.

Female Reproductive Tract

Decysin, a New Member of the Metalloproteinase Family, Is Regulated by Prolactin and Steroids During Mouse Pregnancy1

Nathalie Baran, Paul A. Kelly, and Nadine Binart2

INSERM Unité 344, Endocrinologie Moléculaire, Faculté de Médecine Necker, 75730 Paris Cedex 15, France


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
More than 300 separated actions have been attributed to prolactin (PRL), which could be correlated to the quasi-ubiquitous distribution of its receptor. Null mutation of the PRL receptor (PRLR) gene leads to female sterility caused by a failure of embryo implantation. Using the PRLR knockout mouse model and the mRNA differential display method, among 45 isolated genes, we identified UA+4 as a PRL and steroids-target gene during the peri-implantation period that encodes the decysin. Hormonally regulated in the uterus during pregnancy, this new member of disintegrin metalloproteinase is present in the uterus at the site of blastocyst apposition in nondifferentiated stromal cells at the antimesometrial pole and, interestingly, is colocalized with the PRLR. At midpregnancy, decysin expression persists specifically at the foeto-maternal junction around vessels. Although it has been previously suggested that decysin expression is related to immune function, its function during pregnancy remains to be clearly established.

decysin, pregnancy, prolactin receptor, steroids


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Embryo implantation is a complex process involving cross-talk between maternal and embryonic cells in which steroids play a critical role [1, 2]. In the rodent, the first conspicuous sign of implantation is an increased endometrial vascular permeability at the site of blastocyst apposition [3, 4]. In response to embryonic implantation, decidual transformation of the endometrium is accompanied by neovascularization, which ultimately leads to the formation of maternal vessels in the placenta. Pregnancy is under the control of growth factors [5–9], cytokines [10, 11], or prolactin (PRL) [12–14]. The prolactin receptor (PRLR) is expressed in the ovary [12, 15] as well as in decidual cells [13, 16] and regulates the expression of local genes possibly by an autocrine mechanism, as in placenta [17].

Female PRLR knockout mice are sterile because of a failure of implantation [18]. The basis of the sterility of PRLR knockout mice is attributed to the absence of sufficient P4 to support implantation and subsequently placental development and maintenance. The rescue of implantation failure in PRLR knockout mice is possible by P4 supplementation [19]. Although implantation occurs, the maintenance of a full-term pregnancy is not complete, with major embryonic loss occurring midpregnancy. We have demonstrated that implantation and decidualization defects in PRLR knockout mice are mediated by ovarian, but not uterine, PRLR [20]. Nevertheless, ovarian steroid deficiencies are not sufficient to explain the failure of pregnancy in PRLR knockout mice, although PRL could play a direct or indirect role on maintenance. Overall these observations indicate that preventing PRL action by disruption of the PRLR gene alters the maternal-decidual transformation in response to the implanting blastocyst, demonstrating an essential role of PRL in reproduction. However, given the complexity of the peri-implantation period, hormone regulation, and gene regulation, the exact molecular events during early pregnancy are still not well understood.

Excluding the mammary gland, the targets of PRL are not clearly defined in the reproductive tract. Using this unique PRLR knockout mouse model we applied the mRNA differential display (DD) method [21] to identify PRL target genes at the peri-implantation period. This report describes the isolation and characterization of one of these genes, UA+4, during pregnancy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Mice

PRLR knockout mice previously generated in our laboratory [18] were maintained two per cage at 25°C and 80% relative humidity with a 12L:12D cycle and fed a pelleted diet ad libitum. Heterozygous female mice were mated with heterozygous males in a pure 129/Sv background. The morning of a vaginal plug detection was designated Day 0.5 of pregnancy. A subgroup of PRLR knockout females received a progesterone (P4) pellet (25 mg; Innovative Research of America, Toledo, OH) supplementation from Day 0.5 to rescue the implantation process and subsequent pregnancy as described previously [19]. On the other hand, wild-type and PRLR knockout mice were ovariectomized and allowed to recover for 2 wk. Groups of five mice were treated with steroids or PRL. The treatment schedule was the following: ovine PRL (0.5 mg, NIAMMD-oPRL-16; a kind gift of the National Hormone and Pituitary Program NID, Bethesda, MD), progesterone (1 mg; Sigma Chemical Co., St. Louis, MO), or estradiol-17ß (100 ng; Sigma), and a combination of both steroids (1 mg P4 and 100 ng E2) diluted in sesame oil. All mice were killed 24 h after subcutaneous injection.

All experimental designs and procedures are in agreement with the guidelines of the animal ethics committee of the Ministère de l'Agriculture.

Tissue Preparations

Wild-type, PRLR knockout, and P4-treated PRLR knockout uteri were collected on Day 5.5 of pregnancy and fresh frozen for mRNA differential display. Whole uteri were also collected from Days 0.5 to 12.5 of pregnancy to analyze the temporal expression of the gene. On Day 5.5, implantation sites were localized by i.v. injections of 0.1 ml Chicago Blue dye solution (1% in saline) and were separated from interimplantation sites and frozen separately.

Differential Display Screening

Total RNA was extracted from uteri by a standard guanidinium thiocyanate-phenol-chloroform procedure [22]. Reverse transcription of mRNA (RT-PCR) and PCR amplification were performed using 33P-labeled nucleotides and primers from an RNA image kit 1 (GenHunter Corporation, Nashville, TN), providing 24 primer combinations for each sample [21]. After extraction and reamplification of the differentially expressed cDNA, a standard Northern analysis was performed to confirm the gene-specific expression using reamplified PCR products as probes. The bands giving differential expression patterns were subcloned into PCR 2.1 vector (Invitrogen, Carlsbad, CA) and sequenced with a dye terminator kit using the ABI Prism System (Perkin-Elmer, Wellesley, MA).

Northern Blotting

Total RNA (7 µg) was electrophoresed on a denaturing 1% agarose gels and transferred to a nylon membrane (Hybond N+, Amersham Pharmacia Biotech, NJ), then UV cross-linked. Membrane prehybridization was performed at 42°C for 3 h in a formamide/SSPE buffer, then hybridized with the labeled probe overnight at 42°C. Probes were synthesized from specific cDNA (25 ng) using the Rediprime II kit and [{alpha}-32P]dCTP (50 µCi/reaction, Amersham). Unincorporated nucleotides were removed with microspin columns. Moreover, membranes were hybridized to a ribosomal protein L-7 (RPL-7) probe to normalize the expression between samples. Membranes were washed three times for 10 min at 42°C with 5 x SSPE/0.5% SDS, 10 min at 42°C with 0.5 x SSPE/0.1% SDS, and then 30 min at 50°C with 0.1 x SSPE/0.1% SDS. Results were visualized by autoradiography and analyzed on Storm 840 (Molecular Dynamics, Inc., Watertown, MA).

Semiquantitative RT-PCR Analysis

Analyses of gene expression levels in ovariectomized mice were performed by semiquantitative RT-PCR. Two micrograms of total RNA were reverse transcribed using oligo-poly(dT) reverse primer and M-MLV reverse transcriptase (Gibco BRL, Carlsbad, CA). The amplification of UA+4 cDNAs was generated with the following specific upper and lower primers (5'-CAAAAACCAATGAATGAAGC-3', 5'-TCTTTGTTCCTGAGGCGTAG-3') using Taq polymerase (Gibco BRL) and 1 µl of the RT reaction. An increasing number of cycles was tested to assess the best conditions to achieve linear amplification. The thermal cycling parameters consisted of 22 cycles of denaturing (45 sec, 94°C); annealing (1 min, 57°C); and extension (45 sec, 72°C). The reaction products were separated on 1.5% TBE agarose gels and stained with ethidium bromide. Results were analyzed with a DC digital camera (Eastman Kodak, Rochester, NY) coupled with Kodak ID 2.02 software. In parallel, two primers (5'-GAGGGATCTCGCTCCTGGAAGA-3', 5'-GGTGAAGGTCGGAGTCAACGGA-3') corresponding to glyceraldehyde 3-phosphate dehydrogenase (GAPDH) were included in a separate PCR reaction for each experiment as internal control.

In Situ Hybridization

The original clone UA+4 was removed from pCR2.1 by restriction digestion using EcoRI, purified, and subcloned into the pGEM3Z vector. This vector was used to prepare sense or antisense RNA probes with T7 or SP6 polymerase (Promega, Madison, WI). The single-stranded RNA transcripts were libeled with [{alpha}-35S]UTP (Amersham) resulting in probes with a specific activity of 2 x 109 dpm/µg.

Uteri at Days 5.5 and 12.5 were embedded in OCT and frozen in cold isopentane. Frozen sections (8 µm) were placed onto superfrost gold slides and then fixed in 4% paraformaldehyde in PBS for 10 min at room temperature. Following prehybridization, sections were hybridized to cRNA probes for 18 h at 53°C in a humidified box for 16–18 h in 50% deionized formamide/0.3 M NaCl/20 mM Tris-HCl (pH 8.0)/5 mM EDTA/10 mM NaPO4 (pH 8.0)/10% dextran sulfate/1X Denhart 0.5 mg/ml yeast RNA. After hybridization and washing, the sections were incubated with ribonuclease A (10 µg/ml) at 37°C for 15 min, then dehydrated and exposed to NTB-2 liquid Kodak emulsion for 1–3 wk. The slides were poststained with hematoxylin.

Statistical Analyses

Densitometric analysis of the intensity of the signals from Northern blots was determined by Image quaNT (Molecular Dynamics, Sunnyvale, CA). The different levels between samples were normalized according to housekeeping gene RPL-7.

Densitometric analysis of the signal intensity from the semiquantitative RT-PCR products was determined with a DC120 digital camera (Kodak) coupled with Kodak 1D 2.0.2 software. Values of each band were normalized to GAPDH for the same sample.

The data were reported as means ± SEM and were subjected to a one-way ANOVA followed by pairwise comparison procedures or multiple comparisons to determine differences between groups using the Statview package (SAS, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Identification of a Disintegrin Metalloproteinase As a PRL-Regulated Gene

To identify PRL-regulated genes in uteri during the peri-implantation period, we applied the mRNA differential display technique to three experimental conditions. We compared gene expression patterns in wild-type, PRLR knockout and P4-treated PRLR knockout uteri from Day 5.5 of pregnancy. Among 45 PRL-regulated genes isolated [23], we selected UA+4, a transcript isolated from wild-type mouse that was also expressed in the P4-treated knockout mice (Fig. 1A). The extracted band was labeled and used as a probe on a Northern blot containing the initial RNA populations used for the mRNA differential display. UA+4 hybridized to a transcript of ~2.2 kb (Fig. 1B). The clone of 487 bp was sequenced and analyzed in BLAST/UniGene and was found to be homologous (99%) to mouse decysin mRNA (accession AJ242912) [24], already cloned in human and then in mouse, and mostly reported as expressed in smooth muscles. This gene encodes a disintegrin metalloproteinase protein (467 aa, CAB54557) representing a new member of a disintegrin and metalloproteinase (ADAM) family. This protein contains a disintegrin domain responsible for cell adhesion and a metalloproteinase catalytic domain.



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  		FIG. 1. Isolation and identification of UA+4 gene at Day 5.5 in uteri. A) Differential display of uterine mRNAs at Day 5.5 of pregnancy. Three different RNA samples from wild-type, PRLR knockout (KO), and P4-treated knockout (KO+P4) mice on Day 5.5 were compared by differential display. The arrow indicates the position of the UA+4 band. B) The PCR amplified cDNA fragment UA+4 was subsequently cloned. Northern blot hybridization of the uterine RNA samples (7 µg) used for differential display was performed with a cDNA probe corresponding to the UA+4 clone, which was hybridized to a ~2.2 kb mRNA and then normalized to RPL-7 as the internal control.

Uterine Expression of Decysin

Decysin mRNA expressions are not different in prepubertal and pubertal mice of both genotypes. During early pregnancy, decysin expression is not greatly modified, whereas a modulation of expression was shown from Day 1.5 of pregnancy in wild-type mice. In whole uteri from Day 5.5 of pregnancy in wild-type and P4-treated knockout mice (Fig. 2A), an increase of expression was observed in both wild-type (P < 0.03) and P4-treated knockout mice (P < 0.05) compared with Day 3.5. These results suggest that P4 regulates the decysin gene expression during the peri-implantation period of pregnancy. Interestingly, at midpregnancy decysin expression was important for both genotypes and significantly increased for wild-type uteri. Furthermore, the decysin transcript is preferentially expressed at the blastocyst site of implantation compared with the interimplantation site (Fig. 2B) for both genotypes. Nevertheless, decysin expression remains at the same level on both Days 5.5 and 12.5 in P4-treated knockout mice even though its level increased significantly (P < 0.03) in wild-type sites. At Day 12.5, the decysin expression was higher in the wild-type site than in the P4-treated knockout site (P < 0.03). These observations showed that the decysin gene was differentially regulated during pregnancy, particularly at the implantation site and from midpregnancy.



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  		FIG. 2. Decysin mRNA expression in the uterus. A) Expression of results from Northern blot analysis from wild-type (solid line), knockout (dotted line), and P4-treated (dashed line) uteri. Seven micrograms of total RNA were isolated from whole wild-type, knockout, and P4-treated uteri of prepubertal or pubertal mice and at the different periods of pregnancy, separated, transferred to nylon membrane, and hybridized sequentially to 32P-labeled UA+4 and RPL-7 probes. B) Results of Northern blot analysis from wild-type (white) and P4-treated knockout (grey) mice embryo implantation sites (S) and interimplantation sites (I) were separated at Days 5.5 and 12.5. All results are means ± SEM of three to 33 individual experiments and normalized to RPL-7. *P < 0.05, **P < 0.03

Effect of Steroid Hormones and PRL on Decysin mRNA in the Uterus

Because steroid hormones are essential for the preparation and maintenance of pregnancy, we examined whether uterine decysin expression was modulated by steroids and PRL (Fig. 3). Therefore, wild-type and PRLR knockout ovariectomized females, withdrawn for 2 wk, were treated with oil alone as controls and with PRL or steroids. After PRL administration, decysin mRNA expression analyzed by semiquantitative RT-PCR was decreased in wild-type mice, whereas no change appeared in PRLR knockout mice as expected. The addition of estradiol (E2) strongly repressed its expression in wild-type as well as in knockout mice, whereas progesterone (P4) administration decreased markedly its expression in wild-type mice only. The combined effect of P4 and E2 treatment leads to an additive response of both steroids in both genotypes. Altogether, these results showed that decysin was strongly controlled by steroids and PRL.



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  		FIG. 3. Effects of PRL and steroids on uterine expression of decysin in ovariectomized mice. Groups of five adult wild-type (white) and five PRLR knockout (black) ovariectomized mice were given a single injection of oPRL, or E2, and/or P4 and killed 24 h later. Mice injected with oil served as a control. Uteri were removed and RNA was extracted. Two micrograms of total RNA were used for a reverse transcription (RT) and the subsequent PCR reaction was performed using the specific UA+4 primers. Data are expressed relative to the control value found in wild-type uteri after oil injection (fixed at 100%)

Localization of Decysin in Pregnant Uteri on Days 5.5 and 12.5

To determine the expression of decysin in a cell-type specific manner, in situ hybridization was performed. First, in the uterus at Day 5.5 of pregnancy, decysin mRNA was detected solely at the antimesometrial pole in wild-type (Fig. 4, A and B) as well as in P4-treated knockout uteri (data not shown). Second, at Day 12.5 where placentation occurred, decysin expression was precisely localized in the spongiotrophoblast and around maternal vessels (Fig. 4, C and E). No specific autoradiographic signal was detected when uterine sections were hybridized with the sense probe as control (Fig. 4, C and F).



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  		FIG. 4. Localization of decysin mRNA in uteri at Days 5.5 and 12.5 of pregnancy. In situ hybridization was performed with the UA+4 antisense (B and E) or sense (C and F) probe at the site of implantation on wild-type uteri at Day 5.5 (A, B, and C) and Day 12.5 (D, E, and F) of pregnancy. Dark-field exposure shows decysin transcripts highly expressed in stromal cells (str) at the antimesometrial pole (am.p) on Day 5.5 (B) and in spongiothrophoblast (s) and the peripheral maternal venous plexus on Day 12.5 (E). Corresponding bright-field micrographs are shown in (A) and (D). em, embryo; m.p, mesometrial pole; m, mesometrium; d, decidua; l, labyrinth. Bar: 500 µm


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Blastocyst implantation in rodents is controlled by numerous growth factors, cytokines, and the synergistic action of both ovarian steroids, estrogen and progesterone [3, 4, 25–27]. There is no evidence that the cytokine PRL plays any role [13, 28] despite the presence of PRLR in the antimesometrial pole of the pregnant uterus [20]. For instance, PRL regulates {alpha}2-macroglobulin in the mesometrial decidua, thus acting in a paracrine manner [29], as does the estrogen receptor ß [30, 31]. In the PRLR knockout model, the implantation defect could be partially rescued by progesterone treatment.

Because the precise mechanisms by which PRL acts within the uterus remain unclear, our investigation was focused on the identification of PRL target genes in the uterus at early stages of pregnancy using the PRLR knockout mouse model. We isolated the decysin gene by the mRNA differential display method. This gene is up-regulated in the uterus at the implantation stage and is especially expressed in the stromal cells during peri-implantation. This is the first report demonstrating cell-specific expression of decysin mRNA in the mouse uterus during pregnancy, thus providing evidence that decysin could be important for the peri-implantation period and the development of placenta. Recently, a dual screening strategy was performed to analyze the expression of 10 000 mouse genes by microarray analysis to obtain a global view and identify novel pathways of implantation [32]. The comparison of implantation and interimplantation sites revealed that decysin was up-regulated in intersites. According to this result, at Day 5.5 the decysin gene exhibits a significantly decreased expression at the wild-type implantation site, whereas it is not significantly different in P4-treated knockout mice. Decysin was initially cloned from dendritic cells of human tonsils [24] and codes for a new member of mammalian disintegrin and metalloproteinase belonging to the ADAMs family, but its function remains unknown [33]. The large family of mostly membrane-anchored proteases have an adhesive function for cell-surface proteins through the C-terminal disintegrin domain and a potential antiadhesive and/or cleavage function through the zinc-dependent metalloproteinase domain, encoding diverse functions such as the activation of receptors and cytokines [34, 35]. For example, gelatinase B is implicated in maternal-embryonic boundary interactions during mouse embryo implantation and remodeling of the uterus [36–38], and ADAMTS-1 acting in follicular rupture is also involved in the regulation of angiogenesis and inflammatory reactions [39–41].

The present study shows for the first time that decysin is present and regulated in a cell-type specific manner in uteri under the influence of both steroid and PRL during pregnancy. In pregnant uteri, the pattern of decysin expression peaks from Day 5.5 to Day 12.5 and agrees with the pattern of angiogenesis [42]. Decysin transcript is specifically detected at the antimesometrial pole in undifferentiated stromal uterine cells at Day 5.5 of pregnancy. This expression is similar to that of PRLR knockout mice and is consistent with observations of Northern blot analysis [20, 43]. Such spatially and temporally restricted expression suggests that paracrine factors as PRL induce decysin expression in maternal cells in the rodent.

It appears that progesterone, which is sufficient to rescue the implantation of embryos but not to recover full pregnancy, induces decysin mRNA expression. The period of Day 12.5, where a dramatical increase of decysin in wild-type sites regulated by PRL is observed, coincides with the timing of placental development as an endocrine organ for hormone and nutriment exchanges between fetus and maternal compartments. At this stage, decysin mRNA is localized around the umbilical vein and maternal vessels at the limit of the labyrinth and decidua, which is termed the spongiotrophoblast. The success of pregnancy depends in part on the success of vascularization at implantation sites and placental development. The observation of smaller embryos from PRLR knockout mice in utero (data not shown) is probably associated with a loss of vascular permeability; a defect of the establishment of vascularization is consistent with our hypothesis. Decysin may play a major role in PRL-dependent angiogenesis in the uterine endometrium. It has been shown recently that E2 and P4 are mediated by the differential temporal expression of proangiogenic factors in the uterus during pregnancy [44]. Perhaps PRL and estrogen could also have a synergistic effect, since estrogen is well known to regulate angiogenesis [45] as PRL in vascularization and immunoregulation. The role of decysin is as yet not clear, and it will be interesting to determine the precise role of decysin during pregnancy.


   ACKNOWLEDGMENTS
 
We are grateful to Prune Imbert-Bolloré for suggestions and Cécile Kedzia for advice with in situ hybridization.


   FOOTNOTES
 
1 Supported in part by grants from INSERM, la Fondation pour la Recherche Médicale, Organon FARO 61/subv.99, and ARC 9952. Back

2 Correspondence: Nadine Binart, INSERM U-344, Faculté de Médecine Necker Enfants malades, 156 rue de Vaugirard, 75730 Paris Cedex 15, France. FAX: 33 1 43 06 04 43; binart{at}necker.fr Back

Received: 27 August 2002.

First decision: 10 September 2002.

Accepted: 5 December 2002.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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