Hum. Reprod. Advance Access originally published online on August 17, 2007
Human Reproduction 2007 22(10):2733-2742; doi:10.1093/humrep/dem208
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Regulation of C-C motif chemokine ligand 2 and its receptor in human decidual stromal cells by pregnancy-associated hormones in early gestation
1 Laboratory for Reproductive Immunology, Hospital and Institute of Obstetrics and Gynecology, Fudan University Shanghai Medical College, Shanghai 200011, People's Republic of China 2 Department of Obstetrics and Gynecology, The Affiliated Hospital, Hainan Medical College, Haikou 570102, People's Republic of China
3 Correspondence address. Tel: (+0086)021-63457331; Fax: (+0086)021-63457331; E-mail: djli{at}shmu.edu.cn
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Abstract |
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BACKGROUND: Decidua is in close contact with the fetal trophoblasts, and involved in immune relationship of mother to fetus. However, the roles of decidua and decidual stromal cells (DSC) in materno-fetal immune regulation remain to be elucidated. In the present study, the expression and regulation of chemokines and their receptors in decidua and DSCs were investigated.
METHODS AND RESULTS: The transcription of 18 chemokine receptors in human first-trimester decidual tissue and DSC were first analysed by RT-PCR. Among these receptors, C-C motif chemokine receptor-2 (CCR2) was highly transcribed. It was demonstrated by RT-PCR and immunostaining that both CCR2 and its major ligand, C-C motif chemokine ligand 2 (CCL2, monocyte chemoattractant protein-1), were expressed in decidua and DSC. We then detected CCL2 in the supernatant of primary cultures of DSC by enzyme-linked immunosorbent assay. It was shown that DSC secreted CCL2 spontaneously and continuously over 72 h (21.72 ± 2.34 ng/ml), and the CCR2 antagonist RS102895 and an inhibitor of the map kinase kinase/mitogen-activated protein kinase (ERK/MAPK) signal pathway decreased significantly the CCL2 secretion of DSC (both P < 0.05). We further studied effects of the pregnancy-associated hormones, estrogen, progesterone or HCG on CCL2 secretion by DSC. CCL2 secretion by DSC was up-regulated by estrogen, progesterone or HCG.
CONCLUSIONS: CCR2 and CCL2 are co-expressed by human first-trimester DSC and decidual tissue. CCL2 is secreted in an autocrine manner through the ERK/MAPK pathway, and is up-regulated by the pregnancy-associated hormones, estrogen, progesterone and HCG, which suggests that CCL2 may play an important role at materno-fetal interface.
Key words: decidual stromal cells/C-C motif chemokine ligand 2/C-C motif chemokine receptor-2/materno-fetal interface/immune regulation
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Introduction |
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Decidualization is the earliest uterine adaptations to pregnancy (Bell, 1983
; Glasser, 1991). Decidual tissue, the maternal component at materno-fetal interface, is composed predominantly of decidual stromal cells (DSC) (Bulmer, 1995). Not only is the DSC classically considered to be nutritious to embryo because of their high glycogen content, but also involved in a series of immune regulations such as production of cytokines (Dudley et al., 1993), and antigen phagocytosis and presentation (Olivares et al., 1997; Ruiz et al., 1997). At the same time, a large and specific population of decidual lymphocytes infiltrate constitutively into the decidua. Although the decidua is an important tissue structure at materno-fetal interface, the roles of decidua in materno-fetal immune regulation remain to be elucidated. Recent studies have shown that the endometrium is able to produce chemokines, such as C-C motif chemokine ligand 7 (CCL7), CXCL8 and CCL4 (Jones et al., 2004). So we propose that the decidua may be a source of chemokines and express the corresponding receptors.
We have proved that chemokines and chemokine receptors are involved in materno-fetal immune regulations (Wu et al., 2004, 2005; Huang et al., 2006). Among the 
50 human chemokines, CCL2 (monocyte chemoattractant protein-MCP-1) is the first C-C motif chemokine identified, and mediates its cellular effects through its binding to C-C motif chemokine receptor-2 (CCR2) and activating different mitogen-activated protein kinase (MAPK) cascades (Dubois et al., 1996). CCR2/CCL2 recruits monocytes/macrophages, T cells, basophils, mast cells and natural killer (NK) cells for infiltration into sites of inflammation (Oppenheim, et al., 1991; Proost, 1996; Gu, 1997). In female, CCL2 expression has been found in endometrial cells during the menstrual cycle and in luteal tissue, involved in an influx of macrophages which takes place in endometrium and the corpus luteum. In response to CCL2 release, the accumulation of macrophages is consistent with their role in the rapid destruction of the corpus luteum during structural luteolysis. CCL2 may act as an inflammatory mediator during luteal regression (Arici et al., 1995; Garcia-Velasco et al., 1999; Penny, 2000).
In the present study, we analysed first the transcription of 18 chemokine receptors in human decidua and DSC of the first-trimester gestation by RT-PCR, and found that CCR2 was highly transcribed. And then, CCL2, the major ligand of CCR2, were found highly transcribed and translated. Furthermore, the autocrine and hormonal regulation of CCL2 secretion by DSC was investigated.
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Materials and Methods |
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Decidual tissue collection
Decidual samples were from elective terminations of the first-trimester pregnancies (6–11 week of gestation) for non-medical reasons at Hospital of Obstetrics and Gynecology, Fudan University. The project was approved by the Fudan University Human Investigation Committee, and informed consent was obtained from each patient.
Isolation and culture of DSC
The DSC were isolated according to the methods of Loke and Singh (Loke et al., 1989; Singh et al., 2005). Decidual tissues from different patients, carefully freed from trophoblast, were fully washed in Ca2+Mg2+-free phosphate-buffered saline (PBS) with 100 U/ml penicillin and 50 µg/ml gentamicin, and minced. The minced tissues were left in a solution of 0.25% trypsin/0.025% EDTA (Invitrogen, USA) for 10 min at 37°C for four times. The enzymatic reaction was stopped by adding cold RPMI 1640 medium (GIBCO, USA) with 20% fetal calf serum (GIBCO). The suspension was filtered through sterile gauzes (100 and 300 µm), and centrifuged at 400gx10 min. The supernatant was discarded, and the cell pellet was suspended in PBS solution and centrifuged on a discontinuous gradient of 20, 40 and 60% Percoll (Amersham, USA) for 20 min at 800g. The cells were collected from the 20/40% interface containing mainly DSC, suspended in RPMI 1640 and washed, and cultured in the complete RPMI medium with 10% fetal bovine serum (FBS) (GIBCO). After primary culture for 30 min, the non-adherent lymphocytes were removed by washing, leaving a highly purified population of DSC free of leukocytes. Immunocytochemistry showed that the vimentin-positive cells (i.e. mesenchymal cells) made up for >98% of cells, while the endothelial cells and cytokeratin-positive epithelial cells were <2%.
Flow cytometry
The purified DSC were cultured for 48 h, treated with trypsin and transferred into plastic tubes. DSCs were washed, suspended in PBS and incubated in PE-cy5.5 CD45 (CALTAG, American) and vimetin-fluorescein isothiocyanate (sc-32 322, Santa cruz) for 30 min at room temperature, with FIX and PERM cell permeabilization reagents (CALTAG Laboratories) according to the instructions. Next, the cells were washed and suspended in PBS and immediately analysed by a flow cytometer (FACSCalibur, BD). The isotypic control antibodies were used.
RT-PCR for chemokine receptor transcription
Total RNA was extracted from human decidual tissues and the cultured DSC with Tri reagent (Molecular Research Center, USA). The complementary DNA (cDNA) was generated with oligo(dT)18 primers using Revert AidTM First Strand cDNA Synthesis Kit (Fermentas Life Science, USA). The 50 µl PCR amplification of the single-strand cDNA was performed by 35 cycles of denaturation (94°C) for 60 s, annealing (55°C) for 30 s and elongation (72°C) for 30 s using 2.5 U Taq polymerase (Fermentas Life Science). The primer sequences are indicated in Table 1. The amplified DNA was fractionated by 2% agarose gel (Oxiod, UK) electrophoresis, and ethidium bromide-stained bands were photographed.
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Immunostaining
For immunohistochemistry, paraffin sections (5 µm) of early human decidua were dehydrated in Tris-buffered saline (TBS), and incubated with hydrogen peroxide and 1% bovine serum albumin (BSA)/TBS to block endogenous peroxidase. Then the samples were incubated with goat anti-human CCR2 antibody (10 µg/ml, ab1668, Abcam) or mouse anti-human CCL2 antibody (25 µg/ml, MAB279, R&D Systems) or goat immunoglobulin (Ig)G or mouse IgG overnight at 4°C in a humid chamber. After washing three times with TBS, the sections were overlaid with peroxidase-conjugated goat anti-mouse IgG (04-18-06, KPL) and rabbit anti-goat (14-13-06, KPL), and the reaction was developed with 3,3-diaminobenzidine (DAB), and counterstained with haematoxylin. The immunohistochemical results were evaluated by a pathologist. The experiments were repeated five times.
For immunocytochemical staining, DSC growing on coverslips was cultured for 48 h. The coverslips were fixed in 4% paraformaldehyde for 20 min at room temperature, washed in PBS and permeabilized for 10 min with 0.25% Triton-100 in PBS. The cells were then incubated with 1% BSA in PBS/Tween (PBST) for 30 min to block non-specific binding of antibodies. The primary antibodies diluted in PBST containing 1% BSA were added. Mouse anti-human vimentin monoclonal antibody (1:100, ZA0511, Dingguo, Beijing), cytokeratin-7 antibody (1:100, 18-0234, Zymed Laboratories, USA) and anti-factor VIII antibody (endothelial cell marker) (114-01, ready to use, Dingguo) were used as markers for DSC. The anti-human CCR2 polyclonal antibody and CCL2 antibody were used to detect whether DSCs express CCR2 and CCL2 protein, respectively. The cells were incubated with primary antibody or isotypic control overnight at 4°C, and then incubated with a peroxidase-conjugated secondary antibody for 60 min at 37°C. The slides were stained with DAB, and counterstained with haematoxylin. The experiments were repeated five times.
Treatment of DSC with CCR2 antagonist RS102895 and MAPK inhibitor U0126
The purified DSC were seeded at 1x106 cells/ml in 12-well plates treated with various concentrations of RS102895 (a CCR2 antagonist, 0–500 ng/ml, Sigma Aldrich) and U0126 [map kinase kinase (ERK)/MAPK inhibitor, 30 µm, Cell signalling] in RPMI1640 (GIBCO) containing 10% FBS. 0.1% dimethylsulphoxide (DMSO) was used as control. After 72 h of culture, the supernatant was collected and kept in small aliquots at –20°C until determination of CCL2 by enzyme-linked immunosorbent assay (ELISA).
Treatment of DSC with the pregnancy-associated hormones
DSC was seeded at 1x106cells/ml in 12-well plates and treated with various concentrations of 17-
estradiol (E2) (10–11 M to 10–7 M), or E210–10 M plus estrogen receptor inhibitor-ICI182,780 (10–9 M, Sigma Aldrich), or progesterone (10–11 M to 10–7 M) or HCG (from Sigma Aldrich; 2–10 kU/l) in phenol red-free RPMI (GIBCO) containing 10% dextran-coated charcoal-treated FBS (Hyclone, Logan, UT, USA). The controls were treated with 0.1% DMSO (for E2 and progesterone) and media only (for HCG). In 72 h of culture, the supernatant was collected, and kept in small aliquots at –20°C until determination of CCL2 by ELISA, whereas the cells were dissociated with Trizol and kept at –80°C until analysis by RT-PCR.
ELISA for determination of CCL2 production by DSC
The purified DSC were transferred into plastic culture wells in RPMI/10% FBS (characterized FBS from GIBCO) at 1x105, 5 x105 or 1x106cells/ml. The supernatants were harvested at 12, 24, 48 and 72 h of culture. Each supernatant was centrifuged at 200g and stored at –20°C. Human CCL2 concentration was determined by ELISA kit (BMS281, Bender MedSystems, Austria) according to the manufacture's instruction. The CCL2 assay sensitivity is 2.31 pg/ml, and an intra-assay coefficient of variation is 4.7%.
Quantitative real-time PCR
Triplicate samples containing cDNA prepared as mentioned above, Taqman universal PCR master mix (Applied Biosystems, Foster City, CA, USA), specific primers and fluorescent dye-labelled Taqman MGB probes for CCL2 and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) were mixed, and analysed on an ABI7000 thermal cycler (Applied Biosystems). The cycling conditions consisted of a denaturation step at 95°C for 10 min, 40 cycles at 95°C for 15 s, a 60-s annealing step at 62°C, and finally a holding temperature of 15°C. To determine the amount of gene product present in the sample, cycle time (Ct) was determined. The average Ct value was calculated from triplicate wells for each sample with each primer set. Most duplicate samples varied by <0.5 Ct. The relative gene expression for individual cDNA samples was determined by calculating 
Ct values (Ct) by subtraction of the Ct value for GAPDH primers from the Ct value for CCL2 primers. The relative fold expression of each gene was determined compared with vehicle or medium in each experiment.
Statistics
Data were analysed using one-way analysis of variance and least significant difference (equal variances assumed), or Tamhane's test (equal variances not assumed) was used post hoc for multiple comparisons with Statistical Package for the Social Sciences software version 11.5. Differences were considered as statistically significant if P < 0.05.
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Characterization for the purity of DSC by immunocytochemistry and flow cytometry
After 48 h of culture, we characterized the expression of vimentin, cytokeratin and anti-factor VIII in these cells. As shown in Fig. 1A, the cells we isolated were almost all stained for vimentin, whereas in Fig. 1B and 1C, no cells were found stained with cytokeratin 7 and anti-factor VIII antibody. We observed that the purity of isolated DSC was >98%. The results of flow cytometry showed that
98.25% of cultured DSC expressed vimentin (Fig 2A–C), which was in agreement with immunocytochemistry.
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Transcription of chemokine receptors in human decidual tissue and DSC in early gestation
We analysed the transcription of 18 chemokine receptors in human decidual tissue using PCR primers specific for human chemokine receptors. Our study showed that the chemokine receptors, CCR2, CCR5 and CCR10, were highly expressed in the decidua. The ratios of the band intensities of chemokine receptors to that of GAPDH were 2.06, 1.06 and 1.13, respectively, so the band intensities of these three chemokine receptors were higher than that of GAPDH in each experiment, while CCR3, CCR6, CCR8-9, CXCR1, and CXCR4 were moderately expressed, but chemokine receptors CCR1, CCR4, CCR7, CXCR3 and CXCR5-6 were expressed only in some decidua, and no CXCR2, XCR1 and CX3CR1mRNA were found in any decidua tissue (Fig. 3A and B). Because the decidual tissue is composed predominantly of DSC, transcription of the 18 chemokine receptors was also examined in DSC. The results showed that the Percoll-gradient-isolated DSC expressed moderately CCR1, CCR3, CCR4, CCR6, CCR7, CCR9, CXCR6, XCR and CX3CR1. The CCR2, CCR5 and CCR10 were expressed highly in DSC, similar to decidua (Fig. 3B) and the ratios of the band intensities of chemokine receptors to that of GAPDH were 1.06, 1.02 and 1.31, respectively.
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Human decidua and DSC translated CCR2 and CCL2
After having identified CCR2 transcription in DSC and decidual tissue by RT-PCR, we further analysed CCR2 protein expression in decidua tissue by immunohistochemistry, and in the primary cultured DSC by immunocytochemistry. The results showed a positive staining for CCR2 in the cytoplasm and on the cytomembrane of DSC, and the cytoplasm and cytomembrane of the primary DSC was also positive for CCR2, as seen in Fig. 4.
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Since CCR2 was expressed highly in decidua and DSC, we wondered whether the decidual tissue and DSC also express CCL2. As expected, CCL2 was transcribed highly as well (Fig. 5). Immunohistochemical and Immunocytochemical staining also confirmed that the first-trimester DSC expressed CCL2 protein (Fig. 5). Occasionally, we also found the CCR2 and CCL2 staining on decidual epithelial cells.
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Human DSC secreted CCL2 in autocrine manner through ERK/MAPK signal pathway
Fig. 6 shows that human DSC secreted high levels of CCL2 in the ng/ml range, and in a time-dependent manner, beginning from 12 h and reaching a peak, 21.72 ± 2.34 ng/ml at 72 h (Fig. 6A).
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We assessed whether an autocrine loop participated in CCL2 secretion and whether ERK/MAPK signal pathway was involved in the production of CCL2. DSCs were incubated with or without RS102895, a CCR2 antagonist, or U0126, a ERK/MAPK inhibitor (30 µm) for 72 h. Then, we harvested the supernatant and detected CCL2 levels by ELISA. Blocking CCR2 using an antagonist decreased significantly CCL2 secretion in a dose-dependent manner, and U0126 also inhibited significantly CCL2 production (P < 0.05, Fig. 6B and C).
E2 increased CCL2 transcription and secretion in DSC
We tested whether E2 regulated the secretion and expression of CCL2 in DSCs (Fig. 7). The primary human DSC were treated with 10–11 M-10–7 M E2, and then the supernatant were analysed for CCL2 by ELISA. It was found that E2 up-regulated CCL2 expression (Fig. 7A). The increased transcription of CCL2 was defined as >2-fold at concentrations of 10–11 M-10–9 M compared to vehicle as assessed by real-time quantitative PCR, and the maximal induction occurred at a concentration of 10–10 M E2 (Fig. 7B).
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To test whether the up-regulation of CCL2 was mediated through estrogen receptor, we examined CCL2 secretion and gene expression in the presence and absence of a specific estrogen receptor antagonist, ICI182780 (Fig. 7C and D). It was found the 10–10 M E2-mediated increase in CCL2 production could be inhibited by the antagonist ICI182780, which shows E2 up-regulated the transcription and secretion of CCL2 in DSC through E2 receptor.
CCL2 secretion of DSC was regulated by progesterone and HCG
Recognizing that progesterone levels increase, and syncytiotrophoblasts secret HCG during pregnancy, we tested whether these hormones regulated CCL2 secretion from human DSC.
We observed an increase of CCL2 secretion in response to progesterone treatment (Fig 8A). Although all doses of progesterone and high levels of HCG showed a promotion of CCL2 secretion by DSC, the promotion did not occur in a simple concentration-dependent manner. The levels of CCL2 peaked in 10–9 M progesterone and 8000 U/l hCG.
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Discussion |
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The differentiation of uterine stromal cells into decidual cells (decidualization) is critical for human implantation and establishment of pregnancy. During pregnancy, there is a recruitment of unique lymphocytes into maternal decidua, and these lymphocytes interact with DSC, not only controlling trophoblast invasion, but also protecting the embryo from maternal immune rejection (Moffett-King, 2002
). But the molecules involved in crosstalking between DSC and decidual lymphocytes are still unknown. The chemokines (chemotactic cytokines) are small heparin-binding proteins that direct the movement of circulating leukocytes and activate lymphocytes, so we proposed that chemokine might be the media of crosstalking between DSC and decidual lymphocytes.
Therefore, in this present study we have investigated expression of the chemokines and chemokine receptors in DSC and decidua tissue from human first-trimester gestation. Here we reported that several chemokine receptors were expressed highly in human decidua and DSC of the first-trimester gestation, especially CCR2. CCR2 and CCL2, the principle ligand for CCR2, were found transcribed and translated in these cells and tissue. Furthermore, DSCs were able to secrete soluble CCL2 into the culture medium in high levels. CCR2 is primarily expressed in almost all circulating monocytes (Charo et al., 1994; Wong et al., 1997). CCL2 is thought to be linked with pathological situations of pregnancy, such as preeclampsia (Jonsson et al., 2006; Lockwood et al., 2006), the inflammation process of parturition (Denision et al., 1998), and preterm labour (Esplin et al., 2005). The CCR2 and CCL2 are not involved in the migration, distribution and activation of uNK cells that are the majority of decidual lymphocytes (Chantakru et al., 2001), and thus CCR2 and CCL2 may be involved in materno-fetal immune regulation, especially playing a role in DSC function. As shown in Fig. 5B, CCR2 was stained more strongly in epithelial cells than in DSCs, which suggests that CCR2 exerts an important role in the association of DSCs with decidual epithelial cells.
In the present study we have demonstrated that human DSC from the first trimester secret CCL2 in an autocrine manner through ERK/MAPK signal pathway. CCL2 mediates its cellular effects through binding to CCR2 and activating different MAPK cascades. While CCL2, through CCR2, promotes CCL2 secretion, CCL2 perhaps also promotes CCR2 expression, which would amplify the autocrine loop and help to stimulate CCL2 secretion and DSC functions, but we need more experiments to prove this.
Pregnancy is characterized by high levels of estrogen, progesterone and hCG, which prompted us to investigate the effect of these pregnancy-associated hormones on the expression of CCL2. Our result has demonstrated that estrogen, progesterone and hCG stimulate CCL2 secretion by DSC. E2 up-regulated CCL2 release, which was dependent upon E2 receptor activity and CCL2 transcription. Even though the majority of studies have observed that estrogen causes a reduction of CCL2 (Pervin et al., 1998; Stork et al., 2002), the present data show that CCL2 protein production by human DSC is really enhanced by E2. Recent studies have suggested that estrogen promotes specifically and preferentially CCL2 expression in spleen and in immature dendritic cells (Bengtsson et al., 2004; Murphy et al., 2004). Our study has also found that progesterone and high levels of hCG promote CCL2 secretion, in agreement with other's finding (Arici et al., 1997a,b; Caballero-Campo et al., 2002; Assmus et al., 2005). Regulatory elements in the promoter regions of the CCL2 gene have been identified by several groups (Ueda et al., 1994,1997; Martin et al., 1997). CCL2 is encoded by a single copy gene, located on chromosome 17 that has a promoter region containing binding sites for AP-1 and for NF-
B. Pregnancy hormones may act through these response elements, and then induce CCL2 transcription and secretion. Our study has demonstrated that the pregnancy-associated hormones may up-regulate CCL2 production by DSC, which appears an important role of CCL2 at materno-fetal interface.
Our previous study has shown that CXCL12/CXCR4 and CXCL16/CXCR6 are involved in materno-fetal crosstalking by recruiting different lymphocytes into decidua, stimulating trophoblast proliferation and invasion (Wu et al., 2004, 2005; Huang et al., 2006). Recent studies suggest that the expression pattern of chemokines may determine the polarization of the immune response to Th1 or Th2 (Sallusto et al., 1997; Bonecchi et al., 1998). Among these chemokines, CCL2 can promote Th2 polarization, and maintain the Th2-dominant milieu (Gu et al., 2000), participating broadly in Th2 responsive disease, such as asthma (Romagnani, 2001). Also, CCL2-deficient mice presented with defective Th2 immunity (Boring et al., 1997). Th2 cytokines, such as interleukin-4, can stimulate the production of CCL2 (Nassu et al., 2001). As known to all, there is a shift in the cytokine pattern from Th1 towards Th2 at materno-fetal interface in a successful pregnancy. Unlike CXCR4/SDF-1 and CXCR6/CXCL16, it is possible that high levels of CCR2 and CCL2 expressed in human DSC may be responsible for the Th2-predominance at materno-fetal interface, which needs our further study to clarify the significance of the chemokine in human decidua. CCR2 was expressed in DSCs, and DSCs secreted CCL2 via CCR2 in an autocrine manner, which suggests that CCR2/CCL2 might be involved in regulation of DSC functions, and DSC may be involved in Th2 predominance via CCL2 secretion.
In summary, we have demonstrated that CCR2 and CCL2 are highly expressed in human decidua and DSCs, and DSCs secret CCL2 in an autocrine manner, which may be up-regulated by the pregnancy-associated hormones, estrogen, progesterone and hCG. Further research is warranted to elucidate the functions and significance of expression of CCL2 and its receptor, CCR2, in decidua, which will lead to a deeper understanding of the crosstalking mechanisms at the materno-fetal interface.
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This work is supported by National Basic Research Program of China 2006CB944009 (D.-J.L.), National Natural Science Foundation of China No. 30670787 (D.-J.L.), and Program for Outstanding Medical Academic Leader (D.-J.L.).
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Submitted on September 4, 2006; resubmitted on June 6, 2007; accepted on June 14, 2007.
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