Molecular Human Reproduction, Vol. 6, No. 3, 246-251,
March 2000
© 2000 European Society of Human Reproduction and Embryology
Uterine physiology |
Effects of lipopolysaccharide and cytokines on production of RANTES by cultured human endometrial stromal cells
Department of Obstetrics and Gynecology, Oita Medical University, Hasama-machi, Oita 879-5593, Japan
Abstract
RANTES (regulated upon activation, normal T cell expressed and secreted), which is a potent chemoattractant for eosinophils, lymphocytes, and monocytes, was recently detected in the human endometrium. The effects of modulators of endometrial function, including lipopolysaccharide (LPS), tumour necrosis factor (TNF)-
, interleukin (IL)-1ß, IL-4 and interferon-
(IFN-), on the production of RANTES by endometrial stromal cells (ESC) were examined by an enzyme-linked immunosorbent assay and Northern blot analysis. The concentration of RANTES in the culture media of non-stimulated ESC was below the level of detection. The concentration of RANTES was increased by the addition of TNF-, IL-1ß and LPS. IFN- synergistically enhanced the TNF-- and LPS-induced RANTES expression, but had no effect on the IL-1ß-induced RANTES expression. The TNF--induced production of RANTES by ESC was inhibited by IL-4. The transcription of RANTES in ESC was also stimulated by TNF-, IL-1ß and LPS in a dose-dependent manner. It is suggested that the LPS and cytokines secreted by the maternal decidual tissue and the developing embryo may regulate the production of RANTES by ESC. The modulation of RANTES concentration in the local environment may contribute to the pathophysiological processes of human reproduction by regulating the immunological reaction at the fetal–maternal interface.
endometrial stromal cell/interferon-/lipopolysaccharide/RANTES/TNF-
Introduction
Human endometrial stromal cells (ESC) reportedly produce and secrete various cytokines. The latter include interleukin (IL)-6 (Nasu et al., 1998a
,b, 1999), IL-8 (Arici et al., 1993; Nasu et al., 1998a,b, 1999), macrophage chemoattractant protein-1 (MCP-1) (Nasu et al., 1998a,b, 1999), macrophage inflammatory protein-1 (MIP-1) (Nasu et al., 1999), tumour necrosis factor (TNF)- (Nasu et al., 1999) and macrophage colony-stimulating factor (M-CSF) (Hatayama et al., 1994; Nasu et al., 1998b, 1999). In addition to the expression of major histocompatibility complex molecules (Komatsu et al., 1998), the expression of these cytokines is suggested to be important in menstruation, bacterial infection, implantation, and in the maintenance of early pregnancy (Tabibzadeh, 1994; Chard, 1995).
Chemokines are a large superfamily of structurally and functionally related molecules with a chemotactic activity that is targeted at specific populations of leukocytes. They are 70–90 amino acids in length, and are divided into two subfamilies according to the position of the first two cysteines which are either separated by one amino acid (C–X–C, ) or are adjacent (C–C, ß) (Miller and Krangel, 1992; Schall, 1992; Baggiolini et al., 1994). A third subfamily with only one cysteine (C) has recently been identified (Kelner et al., 1994). The C–X–C chemokine subfamily includes IL-8, platelet factor 4, ß-thromboglobulin, growth-related oncogene (GRO), and interferon-inducible protein 10, many of which chemoattract and activate the neutrophils (Miller and Krangel, 1992; Baggiolini et al., 1994). In contrast, the C–C subfamily includes regulated upon activation, normal T cell expressed and secreted (RANTES), MIP-1, MIP-1ß, MCP-1, I-309 and HC14, which mainly chemoattract and activate mononuclear cells (Schall, 1992; Baggiolini et al., 1994).
RANTES exhibit chemoattractant activity for monocytes, T lymphocytes, eosinophils and basophils (Schall et al., 1990; Kameyoshi et al., 1992; Schall, 1992) via a C–C chemokine receptor (CCR)1, CCR4 and CCR5 (Gao et al., 1993; Neote et al., 1993; Ben-Baruch et al., 1995; Power et al., 1995; Raport et al., 1996). RANTES is produced by the macrophages, platelets, endothelial cells, fibroblasts, and renal tubular epithelial cells (Heeger et al., 1992; Kameyoshi et al., 1992; Rathanaswami et al., 1993; Devergne et al., 1994; Pattison et al., 1994; Marfaing-Koka et al., 1995).
It has been reported that RANTES is synthesized mainly in the stromal compartment of the normal human endometrium in vivo and in vitro (Hornung et al., 1997). We investigated the effects of known modulators of endometrial function on the expression of RANTES transcript and protein by cultured ESC. We then discuss the regulation of RANTES production in the cytokine network at the fetal–maternal interface in early pregnancy.
Materials and methods
Cell culture conditions
Normal endometrial specimens were obtained from eight pre-menopausal Japanese women who had undergone a hysterectomy for intramural leiomyomas. All specimens were identified as being from the late proliferative stage (days 11–13 of the menstrual cycle) based on standard histological criteria. Normal ESC were separated from the epithelial glands by digesting the tissue fragments with collagenase as previously described (Arici et al., 1993; Nasu et al., 1998a,b, 1999). Briefly, tissue was cut into 2–3 mm pieces and incubated with collagenase (200 IU/ml) (Gibco-BRL, Gaithersburg, MD, USA) in Roswell Park Memorial Institute (RPMI) 1640 medium (Gibco-BRL) with stirring for 2 h at 37°C. The suspension was then filtered through a 150 µm wire sieve to remove mucus and undigested tissue. The filtrate was then passed through a 80 µm wire sieve, which allowed the stromal cells to pass through while the intact glands were retained. After being washed three times with serum-free RPMI 1640, the cells were transferred to culture flasks (Corning, New York, NY, USA) at a concentration of 106 cells/ml in RPMI 1640 supplemented with 10% heat-inactivated fetal bovine serum (FBS; Gibco-BRL), streptomycin (100 IU/ml; Gibco-BRL), and penicillin (100 IU/ml; Gibco-BRL). The culture medium was replaced every 4 days. After three passages (15–20 days after isolation) by standard methods of trypsin treatment, the cells were >98% pure as determined by immunocytochemical staining with antibodies to vimentin (V9; Dako, Glostrup, Denmark), keratin (Dako), factor VIII (Dako) and leukocyte common antigen (2B11+PD7/26, Dako). These cells were used for the experiments. These cells maintained ability of decidualization. The cultures were incubated at 37°C in an atmosphere of 5% CO2 in air at 100% humidity.
Detection of RANTES, IL-1ß and TNF- by enzyme-linked immunosorbent assay (ELISA)
To study the production of RANTES by ESC, 1x106 cells per well were plated onto 6-well culture plates (Corning) in 1 ml of culture medium with 10% heat-inactivated FBS and cultured until fully confluent. The culture media were replaced with fresh culture media that contained various amounts of 12-O-tetradecanoylphorbol 13-acetate (TPA) (0.001–100 nmol/l; Sigma, St Louis, MO, USA), forskolin (1–100 nmol/l; Sigma), lipopolysaccharide (LPS) (0.001–10 µg/ml; Sigma), ethinyloestradiol-17ß (0.1–10 nmol/l; Sigma), medroxyprogesterone acetate (0.1–10 nmol/l; Sigma), the combination of these two steroid hormones, dexamethasone (0.01–10 nmol/l; Sigma), recombinant human IL-1ß (0.001–100 ng/ml; R&D Systems, Minneapolis, MN, USA), recombinant human IL-4 (0.001–100 ng/ml; R&D Systems), recombinant human IL-8 (0.1–100 ng/ml; R&D Systems), recombinant human TNF- (0.01–100 ng/ml; R&D systems), recombinant human transforming growth factor (TGF)-ß1 (0.001–10 ng/ml; R&D systems) and recombinant human IFN- (0.01–100 IU/ml; R&D Systems). In addition, the synergistic effects of recombinant human IFN- with these agents and the effects of IL-4, IL-10, TGF-ß1 and dexamethasone on TNF--induced RANTES production were examined. Under these conditions, the supernatant was collected 0–48 h after stimulation and stored at –70°C until assayed. The cells isolated from one patient were used for each experiment at a time. Each experiment was performed in triplicate and repeated four times. All experiments were performed in the presence of 10% heat-inactivated FBS. To evaluate the involvement of IL-1ß and TNF- in the cytokine- and LPS-induced RANTES production by ESC, the concentrations of IL-1ß in the supernatants of LPS- and TNF--stimulated ESC and those of TNF- in the supernatants of LPS- and IL-1ß-stimulated ESC were also examined.
The concentration of RANTES, IL-1ß and TNF- were determined in the supernatants with commercially available ELISA (R&D Systems). Sensitivity of the assay for RANTES, IL-1ß and TNF- were 5, 1 and 4.4 pg/ml respectively. The maximum intra-assay variation between patient samples was 24.8% when treated with TNF- (10 mg/ml) and IFN- (100 IU/ml) in which the strongest effect on RANTES production was observed.
Preparation of cDNA for RANTES by reverse transcriptase–polymerase chain reaction (RT–PCR)
To prepare the RANTES probe for Northern blot analysis, we isolated cDNA for RANTES from ESC stimulated with TNF- and IFN- by RT–PCR at the outset. Briefly, ESC were cultured on 75 cm2 culture plates (Corning) in 15 ml of culture medium with 10% FBS and cultured until fully confluent. The medium was replaced with fresh culture medium containing 10% FBS and TNF- (10 ng/ml) plus IFN- (100 IU/ml), which are reported to induce RANTES mRNA expression in ESC (Hornung et al., 1997), and cultured for an additional 6 h. Total RNA was extracted from the cells as previously described (Nasu et al., 1999). RANTES transcript was amplified by RT–PCR using an RNA PCR kit with AMV reverse transcriptase (Takara, Tokyo, Japan) as previously described (Nasu et al., 1999). RNA was reverse-transcribed into cDNA.
The PCR primer sets for RANTES (sense primer: 5'-ATGAAGGTCTCCGCGGCACGCCT-3' and antisense primer: 5'-CTAGCTCATCTCCAAAGAGTTG-3') (Matsukura et al., 1996) were synthesized by the phosphoramide method on a DNA synthesizer (Model 8700, Biosearch, San Rafael, CA, USA), and purified on Sephadex G50 columns (Pharmacia LKB Biotechnology) and by high performance liquid chromatography (HPLC). The predicted size of the PCR product was 276 bp.
The cDNA transcribed from 1 µg of total RNA was amplified using a thermal cycler (Model PJ2000, Perkin Elmer, Norwalk, CT, USA) in a total volume of 80 µl containing 4 mmol/l MgCl2, 1x RNA PCR buffer, 0.2 µmol/l of each primer, and 2.5 IU of Taq DNA polymerase (Takara). PCR with primer pairs for RANTES was performed for 35 cycles, with each cycle consisting of a denaturation step of 94°C for 1 min, an annealing step of 61°C for 1 min, and an extension step of 72°C for 1 min. PCR products were separated by 1.5% agarose gel (Takara) electrophoresis and visualized by ethidium bromide (Takara) staining. PCR products were cloned with TA cloning kit (Invitrogen, Leek, The Netherlands) and used as a probe in Northern blot analysis. Direct sequence analysis of the PCR products was performed to verify that the amplified cDNA products were RANTES.
Northern blot analysis of RANTES mRNA
To study the expression of RANTES mRNA in ESC, 1x106 cells were plated on 75 cm2 culture plates (Corning) in 15 ml of culture medium with 10% heat-inactivated FBS and cultured until fully confluent. The medium was replaced with fresh culture medium that contained various amounts of LPS (0.001–1 µg/ml), recombinant human IL-1ß (0.001–100 ng/ml), recombinant human TNF- (0.01–100 ng/ml), recombinant human IFN- (0.01–100 U/ml), and the combination of IFN- with other agents. The cells were then cultured for an additional 0–24 h. Total RNA was extracted as described above. Northern blotting was performed as described previously (Nasu et al., 1999). Briefly, human RANTES cDNA was labelled with [-32P]-dCTP using a random-primed DNA labelling kit (Amersham Life Science, Buckinghamshire, UK). The labelled probe was purified on a Sepharose-G50 column (Pharmacia, Piscataway, NJ, USA). Total RNA (20 µg) was subjected to electrophoresis in agarose/formaldehyde gels and transferred to nylon membranes (Hybond N; Amersham Life Science). Membranes were hybridized to a [32P]-radiolabelled probe for RANTES. Following hybridization, membranes were washed and exposed at –70°C to Kodak XRP-5 film (Eastman Kodak Company, Rochester, New York, USA) with intensifying screens (Eastman Kodak Company). The expression of mRNA for ß-actin was also examined as internal controls. The relative levels of RANTES mRNA were determined by image analysis of the autoradiograms using the public domain NIH image program 1.61 (developed at the U.S. National Institutes of Health). The results are expressed as the ratio of RANTES mRNA signals to the corresponding ß-actin mRNA signals.
Statistical analysis
Data are presented as the mean ± SD of triplicate samples from four separate representative experiments and were analysed by Bonferroni–Dunn test and Student's t-test with StatView 4.5 (Abacus Concepts, Berkeley, CA, USA) as appropriate. P < 0.05 was considered to be statistically significant.
Results
Detection of RANTES, IL-1ß and TNF- in the culture media of ESC
As shown in Figure 1, the concentration of RANTES increased with the addition of increasing amounts of LPS (0.001–1 µg/ml). LPS showed the strongest effect at a concentration of 0.1 µg/ml. The concentration of RANTES increased with the addition of increasing amounts of IL-1ß (0.01–10 ng/ml), with the peak effect seen at 0.1 ng/ml (Figure 2). TNF- increased the secretion of RANTES by ESC in a dose-dependent manner (1–100 ng/ml) (Figure 3). TPA, forskolin, ethinyloestradiol-17ß, MPA, the combination of these two steroid hormones, dexamethasone, IL-4, IL-8, and TGF-ß1 had no effect on RANTES secretion by ESC.
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As shown in Figure 4
, treatment with IFN- alone did not induce RANTES secretion; however, IFN- synergistically enhanced the LPS- and the TNF--induced production of RANTES by ESC (3-fold increase and 6-fold increase respectively). IFN- did not show a synergistic effect on the IL-1-induced RANTES production by those cells.
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The effects of immunomodulatory agents, including IL-4, IL-10, TGF-ß1 and dexamethasone, on the TNF-
-induced production of RANTES by ESC were also examined. IL-4 showed a significant inhibitory effect on TNF--induced RANTES production by ESC. IL-10 weakly inhibited TNF--induced RANTES production by ESC, although the effect did not achieve statistical significance. TGF-ß1 and dexamethasone had no effect on TNF--induced RANTES production by ESC (Figure 5). The concentration of RANTES in the culture medium without cells was below the level of detection. RANTES protein was not detected in the culture medium of non-stimulated ESC incubated for 24 h. The presence or absence of 10% FBS did not affect RANTES production (data not shown).
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The concentrations of IL-1ß in the supernatants of ESC stimulated with LPS, TNF-
, and the combination of IFN- with LPS and TNF- were below the level of detection. Also below the level of detection were the concentrations of TNF- in the supernatants of ESC stimulated with LPS, IL-1ß, and the combination of IFN- with LPS and IL-1ß.
mRNA expression of RANTES in ESC
Sequence analysis of the cDNA fragments amplified by RT–PCR was consistent with the previously reported sequence of human RANTES (Schall et al., 1988) (results not shown). We used this amplified cDNA fragment as a probe for RANTES in Northern blot analysis.
The expression of RANTES mRNA was not detectable in non-stimulated ESC. Expression of RANTES mRNA was induced by LPS (Figure 6), IL-1ß (Figure 7) and TNF-
(Figure 8) in a dose-dependent manner. IFN- (100 IU/ml) synergistically enhanced the TNF- (10 ng/ml)-induced expression of RANTES mRNA in ESC (1.7-fold increase, data not shown).
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Discussion
The RANTES gene and protein expression have been reported in a variety of cell types, including T lymphocytes (Schall et al., 1988), platelets (Kameyoshi et al., 1992), fibroblasts (Rathanaswami et al., 1993), renal epithelial cells (Heeger et al., 1992) and bronchial epithelial cells (Stellato et al., 1995; Manni et al., 1996). The kinetics of RANTES expression differs among cell types; this chemokine is expressed 3–5 days after the activation of peripheral blood T lymphocytes with antigen and mitogen (Schall et al., 1988), while RANTES mRNA rapidly increases in the fibroblasts and epithelial cells stimulated by TNF- and IL-1ß (Heeger et al., 1992; Rathanaswami et al., 1993; Stellato et al., 1995). Our present study demonstrated that RANTES mRNA expression was rapidly induced in ESC. Although the signal transduction of RANTES production has not been fully defined (Nelson et al., 1993, 1996), these findings support RANTES transcription being regulated by different mechanisms in various tissue types, leading to tissue-specific inflammatory processes.
The present study demonstrated that LPS, TNF- and IL-1ß stimulated RANTES mRNA and protein expression by ESC in a dose-dependent manner as previously demonstrated in other cell types (Heeger et al., 1992; Rathanaswami et al., 1993; Devergne et al., 1994; Pattison et al., 1994; Marfaing-Koka et al., 1995; Stellato et al., 1995; Sticherling et al., 1995; Berkman et al., 1996; Li et al., 1996; Manni et al., 1996; Janabi et al., 1999). Treatment with IFN- alone stimulates RANTES production by keratinocytes (Li et al., 1996), airway epithelial cells (Berkman et al., 1996) and macrophages (Devergne et al., 1994), but not by endothelial cells (Marfaing-Koka et al., 1995). IFN- synergistically enhances the LPS- and TNF--induced, but not the IL-1ß-induced, expression of RANTES mRNA and protein production by these cells. It involves the induction of TNF- receptors by IFN- (Ruggiero et al., 1986), the induction of IFN- receptors by TNF- (Sanceau et al., 1992), or the synergy between intracellular events induced by the binding of each cytokine to its receptor. IFN- and TNF- also co-operate to induce the expression of RANTES by various cell types, including keratinocytes (Li et al., 1996), synovial fibroblasts (Rathanaswami et al., 1993), endothelial cells (Marfaing-Koka et al., 1995), microglial cells and astrocytes (Janabi et al., 1999). In addition, IFN- enhances the IL-1ß-induced production of RANTES by synovial fibroblasts (Rathanaswami et al., 1993), microglial cells and astrocytes (Janabi et al., 1999). We previously reported that IFN-, an immunomodulatory T helper 1 (Th1)-type cytokine, stimulates IL-6, MCP-1 and M-CSF expression by ESC, but inhibits IL-8 expression by these cells (Nasu et al., 1998b). An early component of implantation of the fertilized ovum is suggested to be the production of cytokines such as TNF-, IL-1ß and IFN-, by both the embryo and the decidua (Haynes et al., 1993). These cytokines may stimulate cells in the decidua, e.g. fibroblasts, endothelial cells and ESC, to up-regulate RANTES transcription and protein production, leading to the recruitment of macrophages and lymphocytes into the decidua.
Cytokine-induced RANTES production in a variety of cell types has been shown to be inhibited partly by the T helper 2 (Th2)-derived cytokines, IL-4, IL-10, and IL-13, as well as by dexamethasone (Rathanaswami et al., 1993; Marfaing-Koka et al., 1995; Stellato et al., 1995; Berkman et al., 1996). IL-4 inhibited the TNF--induced RANTES production by ESC. It has been suggested that pregnancy is reminiscent of a Th2-dominant situation (Wegmann et al., 1993; Raghupathy, 1997), and that the Th2-type cytokines IL-4, IL-5 and IL-10 are responsible for the Th2 bias in the mouse fetoplacental tissue for the maintenance of pregnancy (Wegmann et al., 1993). In view of this concept, the present data suggest that IL-4, a Th2-type cytokine produced by the embryo (Haynes et al., 1993), may inhibit the excessive production of RANTES via a paracrine mechanism.
In summary, we demonstrated that LPS, TNF- and IL-1ß stimulated, while IL-4 inhibited, the production of RANTES by cultured human ESC. IFN- synergistically augmented the LPS- or TNF--induced production of this chemokine. These observations may provide insights into the mechanism involving the recruitment of inflammatory cells during reproductive processes in humans.
Acknowledgments
This work was supported in part by Ministry of Education, Science and Culture of Japan Grant-in-Aid 30274757 for Scientific Research.
Notes
1 To whom correspondence should be addressed 
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Submitted on June 14, 1999; accepted on December 1, 1999.
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 B. Sun, K. Nasu, J. Fukuda, S. Mine, M. Nishida, and I. Miyakawa Expression of macrophage inflammatory protein-3{alpha} in an endometrial epithelial cell line, HHUA, and cultured human endometrial stromal cells Mol. Hum. Reprod., October 1, 2002; 8(10): 930 - 933. [Abstract] [Full Text] [PDF]
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K. Kai, K. Nasu, S. Nakamura, J. Fukuda, M. Nishida, and I. Miyakawa Expression of interferon-{gamma}-inducible protein-10 in human endometrial stromal cells Mol. Hum. Reprod., February 1, 2002; 8(2): 176 - 180. [Abstract] [Full Text] [PDF]
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J. M. Garcia-Pacheco, C. Oliver, M. Kimatrai, F. J. Blanco, and E. G. Olivares Human decidual stromal cells express CD34 and STRO-1 and are related to bone marrow stromal precursors Mol. Hum. Reprod., December 1, 2001; 7(12): 1151 - 1157. [Abstract] [Full Text] [PDF]
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D. I. Lebovic, V. A. Chao, J.-F. Martini, and R. N. Taylor IL-1{beta} Induction of RANTES (Regulated upon Activation, Normal T Cell Expressed and Secreted) Chemokine Gene Expression in Endometriotic Stromal Cells Depends on a Nuclear Factor-{kappa}B Site in the Proximal Promoter J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4759 - 4764. [Abstract] [Full Text] [PDF]
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K. Nasu, K. Fujisawa, K. Arima, K. Kai, T. Sugano, and I. Miyakawa Expression and regulation of growth-regulated oncogene {alpha} in human endometrial stromal cells Mol. Hum. Reprod., August 1, 2001; 7(8): 741 - 746. [Abstract] [Full Text] [PDF]
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K. Nasu, K. Arima, K. Kai, K. Fujisawa, M. Nishida, and I. Miyakawa Expression of epithelial neutrophil-activating peptide 78 in cultured human endometrial stromal cells Mol. Hum. Reprod., May 1, 2001; 7(5): 453 - 458. [Abstract] [Full Text] [PDF]
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T. Sugano, H. Narahara, K. Nasu, K. Arima, K. Fujisawa, and I. Miyakawa Effects of platelet-activating factor on cytokine production by human uterine cervical fibroblasts Mol. Hum. Reprod., May 1, 2001; 7(5): 475 - 481. [Abstract] [Full Text] [PDF]
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K. Nasu, T. Sugano, K. Fujisawa, K. Arima, H. Narahara, and I. Miyakawa Effects of interleukin-4 on the in-vitro production of cytokines by human endometrial stromal cells Mol. Hum. Reprod., March 1, 2001; 7(3): 265 - 270. [Abstract] [Full Text] [PDF]
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D. Hornung, F. Bentzien, D. Wallwiener, L. Kiesel, and R.N. Taylor Chemokine bioactivity of RANTES in endometriotic and normal endometrial stromal cells and peritoneal fluid Mol. Hum. Reprod., February 1, 2001; 7(2): 163 - 168. [Abstract] [Full Text] [PDF]
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