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Biology of Reproduction 67, 1414-1418 (2002)
© 2002 Society for the Study of Reproduction, Inc.

Regular Article

Decidualization Induces the Expression and Activation of an Extracellular Protease Neuropsin in Mouse Uterus1

Kazumasa Matsumoto-Miyai2,a, Ryoko Kitagawab, Ayako Ninomiyaa, Yoshiharu Momotac, Shigetaka Yoshidad, and Sadao Shiosakaa

a Division of Structural Cell Biology, Nara Institute of Science and Technology, Ikoma, Nara 630-0101, Japan b Department of Laboratory Science, School of Health Sciences, Faculty of Medicine, Kanazawa University, Kanazawa, Ishikawa 920-0942, Japan c Department of Anatomy, Faculty of Medicine, Kagoshima University, Kagoshima, Kagoshima 890-8520, Japan d Department of Anatomy, Asahikawa Medical College, Asahikawa, Hokkaido 078-8510, Japan


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Uterine decidualization is accompanied by the remodeling of the cell-matrix and cell-cell interactions around the endometrial stromal cells to allow an appropriate invasion of trophoblasts. This remodeling is thought to require the proteolysis of extracellular matrix proteins or cell adhesion molecules; however, the molecular mechanism remains poorly understood. In this study, decidualization induced the expression and activation of an extracellular serine protease neuropsin in the mouse uterus. Although nonpregnant uteri contained little neuropsin, the protein content and enzymatic activity increased markedly and peaked at the midgestational period in pregnant uteri. Neuropsin expression and activity was also upregulated in artificially induced deciduomata but not in nondecidualized pseudopregnant uteri. Neuropsin is the first extracellular protease to show the evident induction of expression and activity by decidualization and might contribute to the remodeling of extracellular components after decidualization.

decidua, gene regulation, pregnancy, uterus


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
During pregnancy, maternal and fetal tissues interact structurally, biochemically, and hormonally. Only during pregnancy does such an interaction occur between two different organisms under normal physiological conditions. In common laboratory rodents and humans, the maternal uterus exhibits hormone-mediated growth, differentiation, and the transformation of endometrial stromal cells to decidual cells following the implantation of an embryo [1]. This uterine process, known as decidualization, involves extracellular matrix (ECM) remodeling from interstitial-type ECM to basal laminar-type components around the endometrial cells [2–5] and a dynamic change of cell-cell adhesion [6–9]. Because decidual cells are strategically positioned to counteract the invasion of the fetal trophoblast cells, decidualization accompanied by this remodeling of the cell-matrix or cell-cell interactions serves as protection against excessive invasion by trophoblast cells [10]. The decrease in tensile strength allows expansion in response to uterine growth [1]. The molecular mechanism underlying ECM remodeling during decidualization is of immense interest because it may provide insight into the prevention of invasion by cancer cells as well as the dynamic rearrangement of the extracellular environment.

The remodeling of the decidual cell-matrix or cell-cell interactions is thought to require extracellular proteases degrading ECM proteins and cell adhesion molecules. However, it is not known which protease actually contributes to the extracellular remodeling in decidua. Neuropsin, a serine protease cloned from the mouse hippocampus cDNA library [11], is one candidate for these proteases for the following reasons: 1) neuropsin mRNA was expressed in the decidual cells of glycogen-rich and mesometrial regions during midgestation, whereas no expression was detected in nonpregnant uteri [12]; and 2) neuropsin was activated after release into the extracellular space and cleaved an ECM protein, fibronectin [13]. However, the protein expression of neuropsin in the pregnant uterus remains poorly understood. In addition, the spatiotemporal pattern of mRNA and protein expression of proteases is not necessarily consistent with the expression of their proteolytic activity owing to the rigid regulation of their activity by their specific activator and inhibitor. Neuropsin activity itself is strictly regulated by an activational process after release [13] and by its specific inhibitors [14]. To gain an insight into the neuropsin function in pregnant uteri, we examined the proteolytic activity of neuropsin in addition to its expression. We first investigated the temporal change in the contents of total and active neuropsin protein during normal pregnancy. Neural activity regulates the expression and activity of neuropsin in the brain [15–18], but the mechanisms regulating neuropsin in the uterus are unknown. We then examined the expression and activation of neuropsin in pseudopregnant uteri and artificially induced deciduomata to identify the stimulus (hormonal regulation, decidualization, or signals from the conceptus) inducing its upregulation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Preparation of Uterine Tissues

Female ddY mice were mated and checked for vaginal plugs in the morning (midnight = 0 days postcoitum ["c]). Mice were killed while deeply anesthetized, and uteri were removed at the times indicated. For preparation of nondecidualized pseudopregnant uteri and deciduoma-induced uteri, female mice were mated with vasectomized males. At 4.5 dpc, uteri were induced to decidualize by scratching the left uterine horn with forceps or by transfer of 40–60 µl of peanut oil into the left uterine horn with a 25-gauge needle and a 1-ml syringe under anesthesia. The removal of the left and right uterine horns was carried out at 72 h after scratching or oil injection (7.5 dpc). The swollen left uterine horn was adopted as the deciduoma-induced uterus, and the right nondecidualized pseudopregnant uterine horn was used as a control. The protocols using animals were reviewed and approved by our institutional oversight committee.

In Situ Hybridization Histochemistry

Digoxygenin (DIG)-labeled antisense and sense cRNA probes for neuropsin were prepared using the B41 plasmid covering positions 691–1131 of the neuropsin cDNA and a DIG RNA labeling kit (Boehringer Mannheim, Mannheim, Germany) according to the manufacturer's protocol. The removed uteri were frozen with powdered dry ice. Sections (12 µm thick) were cut on a cryostat and thaw-mounted onto 3-aminopropyltriethoxysilane-treated glass slides. In situ hybridization and visualization of the hybridized probes were carried out according to a conventional method as described previously [19]. Sections processed by DIG-in situ hybridization were counterstained with methyl green.

Measurement of Neuropsin Protein Content

The protein content of neuropsin in the uterus was measured according to a method described previously [16]. The uterus of each animal was homogenized in lysis buffer (50 mM Hepes, pH 7.4, 5 mM EDTA, 0.15 M NaCl, and 1.0% Triton X-100) with a Polytron (Misonix, Farmingdale, NY). The homogenates were centrifuged at 12 000 x g for 30 min to remove debris. The supernatants were precleaned with rabbit anti-rat IgG (Rockland, Gilbertsville, PA) and protein G-Sepharose (Amersham Pharmacia Biotech, Buckinghamshire, U.K.) complex (IgG complex) at 4°C for 30 min. After centrifugation (7 min, 1000 x g), the supernatant was incubated with antineuropsin monoclonal antibody mAbF12 and the IgG complex at 4°C overnight with gentle agitation. After washing with lysis buffer six times, the immunoprecipitates were collected by centrifugation (7 min, 1000 x g). The amidolytic activity of the immunoprecipitated uterine neuropsin was quantified by measuring the fluorescence of the methylcoumarin released from the synthetic substrate Boc-Val-Pro-Arg-MCA (Peptide Institute, Osaka, Japan) after full activation by 200 ng of lysine-specific endopeptidase (Achromobacter lyticus protease 1, EC3.4.21.50; 3.4 AU/ml; Wako Pure Chemicals, Osaka, Japan) at 37°C for 5 min. This activation process was necessary to measure the total protein content, including the precursor form of neuropsin. The process was omitted for the measurement of the active form of neuropsin. This method is highly sensitive and specific for the measurement of neuropsin, as confirmed in a previous study [16, 20]. Because total neuropsin, including its nonactive precursor form, should be represented by protein contents rather than proteolytic activities, the neuropsin activities obtained by this method were converted into protein contents by reference to the activity of standard recombinant neuropsin. To examine how much neuropsin was the active form, active neuropsin activities were also converted into protein contents. Statistical evaluation was performed using an ANOVA with a post hoc Student-Newman-Keuls test. P values of <0.05 were considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Neuropsin Expression and Activity in Normal Pregnant Uteri

In a previous study, an in situ hybridization method with a 35S-labeled cRNA probe revealed neuropsin mRNA in the normal pregnant uterus localized to the decidual cells [12]. To confirm this observation, we performed in situ hybridization using a DIG-labeled cRNA probe (DIG-in situ hybridization) for the exact identification of the positive cell types. Intense positive signals (dark brown) were observed in the glycogen-rich region at 7.5 dpc (Fig. 1A) and in the fully decidualized zone of the mesometrial regions around the embryo at 9.5 dpc (Fig. 1B). At both time points, the antimesometrial region exhibited very faint positive signals. At higher magnification, the cytoplasm of decidual cells exhibited positive signals (arrowheads, Fig. 1C), and fetal trophoblast giant cells were negative (arrows, Fig. 1C). These cells were identified by morphological criteria. Thus, intense positive signals were detected in the decidual cells close to the trophoblast giant cells, i.e., near the boundary between the maternal and embryonic tissues.



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  		FIG. 1. Neuropsin mRNA and protein in normal pregnant mouse uteri. A–C) DIG-in situ hybridization for neuropsin mRNA in normal pregnant uteri at 7.5 dpc (A) and 9.5 dpc (B and C). Positive signals for neuropsin mRNA are dark brown. Panel C is a higher magnification of the boxed area in B. Positive fully decidualized cells are indicated by arrowheads, and arrows indicate negative trophoblast giant cells. All sections were counterstained with methyl green. GL, Glycogen-rich region; M, mesometrial region; AM, antimesometrial region. Bar = 1 mm (A and B) and 0.1 mm (C). D) Total (open bars) and active (shaded bars) neuropsin levels in normal pregnant uteri. The vertical axis indicates the neuropsin protein content per total protein content (pg/g). Values shown are the means of three independent experiments. Error bars indicate SEM. *P < 0.05 versus total neuropsin content in nonpregnant uteri and in pregnant uteri at 4.5 dpc. #P < 0.05 versus active neuropsin content in nonpregnant uteri and in pregnant uteri at 4.5, 12.5, and 14.5 dpc. ANOVA with post hoc Student-Newman-Keuls test.

We also measured the total neuropsin protein content (including the nonactive precursor and active form) and the active neuropsin protein content in normal pregnant uteri at various time points using a highly sensitive and specific method. In nonpregnant uteri, neuropsin protein was scarcely detected (Fig. 1D). By contrast, pregnant uteri showed a marked increase in total neuropsin protein content; it rapidly increased from 4.5 dpc to 6.5 dpc, reached a maximum at 10.5 dpc, and decreased thereafter (open bars, Fig. 1D). Total neuropsin content from 6.5 to 10.5 dpc was significantly higher than that in nonpregnant uteri and at 4.5 dpc (P < 0.05, ANOVA with post hoc Student-Newman-Keuls test; Fig. 1D). However, the active neuropsin protein content showed a transient increase at the midgestational period (shaded bars, Fig. 1D); active neuropsin content at only 6.5 and 8.5 dpc was significantly higher than that of the nonpregnant control and than that at 4.5, 12.5, and 14.5 dpc (P < 0.05, ANOVA with post hoc Student-Newman-Keuls test; Fig. 1D). From 4.5 to 10.5 dpc, almost all neuropsin protein was of the active form, indicating that the enzymatic activity and protein expression were upregulated during pregnancy. At 12.5 and 14.5 dpc, the active neuropsin content decreased to near nonpregnant levels and accounted for about 25% of total neuropsin protein (Fig. 1D). Thus, after 10.5 dpc, neuropsin might be disfunctional because of a reduction in both production and activation. These results suggested that neuropsin actually functioned in the pregnant uterus, particularly in the early to midgestational period.

Neuropsin Expression and Activity in Artificially Induced Deciduomata

The spatiotemporal pattern of neuropsin expression and activation strongly suggested an involvement in the process of decidualization. To examine whether neuropsin is induced by decidualization itself or by signals from the conceptus, we investigated the expression and localization of neuropsin mRNA in artificially induced deciduomata, which exhibit the same morphological [21] and molecular [22, 23] changes as normal decidualization without the invasion of trophoblasts. The pseudopregnant left uterine horn was induced to decidualize by trauma or oil injection, and the noninduced right uterine horn was employed as a nondecidualized control. No positive signal was observed in the nondecidualized pseudopregnant uteri using DIG-in situ hybridization. However, the deciduoma induced by trauma (Fig. 2, A and B) or oil injection (Fig. 2, C and D) showed significant positive signals around the uterine lumen. In both cases, the neuropsin mRNA-positive cells were positioned around a layer consisting of closely packed cells (considered the primary decidual zone, based on morphological criteria) and were large (arrows, Fig. 2, B and D); therefore, these positive cells were considered to be fully transformed decidual cells. The positive signal in the oil-induced more highly decidualized deciduomata (Fig. 2, C and D) tended to be more intense and more extensive than that in the trauma-induced deciduomata (Fig. 2, A and B), suggesting that neuropsin mRNA expression might be correlated with the extent of decidualization.



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  		FIG. 2. Neuropsin mRNA and protein in artificially induced mouse deciduomata. A–E) DIG-in situ hybridization for neuropsin mRNA in the deciduoma induced by trauma (A and B) or oil injection (C and D) and in the nondecidualized pseudopregnant uterus (E). Asterisks (A and C) indicate the uterine lumen. Panels B and D are higher magnifications of the boxed areas in A and C, respectively. Positive cells in B and D are indicated by arrows. All sections were counterstained with methyl green. Bar = 0.2 mm (A and C), 0.05 mm (B and D), and 0.5 mm (E). F) Total (open bars) and active (shaded bars) neuropsin levels in various uteri. The vertical axis indicates the neuropsin protein content per total protein content (pg/g). Values shown are the means of three independent experiments. Error bars indicate SEM. *P < 0.05 versus total neuropsin content in nonpregnant and pseudopregnant uteri; #P < 0.05 versus active neuropsin content in nonpregnant and pseudopregnant uteri. ANOVA with post hoc Student-Newman-Keuls test.

We also examined the neuropsin protein content in the artificially induced deciduomata. The oil-induced deciduomata contained a significant amount of total neuropsin protein, whereas little neuropsin protein was detected in the nonpregnant and nondecidualized pseudopregnant uteri (open bars, Fig. 2F). These data were highly consistent with mRNA expression (Fig. 2, A–E). Most of the neuropsin protein in the oil-induced deciduomata (about 85%) was also of the active form (shaded bars, Fig. 2F). Total and active neuropsin content in the deciduomata was significantly higher than that in nonpregnant and pseudopregnant uteri (P < 0.05, ANOVA with post hoc Student-Newman-Keuls test). These data suggest that not only the expression but the activation of neuropsin was induced by decidualization without a conceptus. Total and active neuropsin protein levels in the oil-induced deciduomata were almost the same as the maximum (at 8.5 dpc) during normal pregnancy (Fig. 2F). The protein levels of total and active neuropsin in deciduomata and in normal pregnant uteri at 8.5 dpc were not significantly different (ANOVA with post hoc Student-Newman-Keuls test). This finding implies that decidualization is sufficient to induce neuropsin protein expression and enzymatic activation and that the presence of a conceptus is not necessary.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, expression and activation of an extracellular protease, neuropsin, was critically regulated by decidualization. Although in previous studies matrix metalloproteinases (MMPs) and plasminogen activators (PAs) were candidate proteases thought to degrade decidual ECM components, these compounds did not show the functional upregulation caused by deciduogenic stimuli; the MMPs expression and activity were unchanged or decreased [24–27], and the regulation of PAs has remained controversial [28–31]. Thus, no protease has previously been reported to be induced by decidualization. Neuropsin is the first extracellular protease showing a transient increase in expression and function induced by decidualization. Neuropsin expression and activity reached a peak when considerable decidualization had already occurred. Therefore, neuropsin might contribute to the extracellular remodeling at the late phase or after decidualization rather than during the transformation into decidual cells.

Our previous studies revealed that neuropsin was involved in synaptic plasticity in the hippocampus [11, 15–18] and in keratinization [32] and wound healing [33] in the skin. During these processes, dynamic changes in cell-matrix and cell-cell interactions take place [34, 35]. Neuropsin cleaves an ECM component fibronectin [13] and synaptic cell adhesion molecules (unpublished results); hence, it might contribute to the decomposition of precedent interactions prior to the establishment of novel ones. Decidual cells also exhibit dynamic molecular remodeling in the extracellular environment after the late phase of decidualization. For example, fibronectin protein content decreased as decidualization progressed, and the reduction was accompanied by changes in the pattern of organization from a fibrillar network to punctate patches [22, 36]. Furthermore, the expression of a cell adhesion molecule, cadherin-11, was increased in the decidua of early pregnancy but was markedly reduced at term [37]. Neuropsin might contribute to the decidualization process by cleaving these molecules.


   FOOTNOTES
 
1 This study was supported by a Grant-in-Aid for Encouragement of Young Scientists from the Japan Society for the Promotion of Science to K.M.-M. Back

2 Correspondence: Kazumasa Matsumoto-Miyai, Division of Structural Cell Biology, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0101, Japan. FAX: 81 743 72 5419; kmatsumo{at}bs.aist-nara.ac.jp Back

Received: 1 April 2002.

First decision: 23 April 2002.

Accepted: 6 June 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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