Molecular Human Reproduction, Vol. 8, No. 1, 68-74,
January 2002
© 2002 European Society of Human Reproduction and Embryology
Uterine physiology |
Differential regulation of copper–zinc superoxide dismutase and manganese superoxide dismutase by progesterone withdrawal in human endometrial stromal cells
Department of Obstetrics and Gynecology, Yamaguchi University School of Medicine, Minamikogushi 1-1-1, Ube 755-8505, Japan
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The present study was undertaken to investigate the role of estrogen and progesterone in the expression of copper–zinc superoxide dismutase (Cu,Zn-SOD) and manganese SOD (Mn-SOD) in human endometrial stromal cells (ESC). ESC were incubated with estradiol (10–8 mol/l), medroxyprogesterone acetate (MPA, 10–6 mol/l), or estradiol + MPA for 18 days. MPA significantly increased Cu,Zn-SOD and Mn-SOD mRNA levels and enzyme activities as well as the mRNA level of insulin-like growth factor-binding protein-1 (IGFBP-1), a marker for decidualization. Estradiol only augmented the effects of MPA on Cu,Zn-SOD activity and IGFBP-1 mRNA level, and estradiol alone had no effect. To study the withdrawal of estrogen and progesterone (EP withdrawal), ESC that had been treated with estradiol + MPA for 12 days were washed and then incubated with or without estradiol + MPA for a further 11 days. Cu,Zn-SOD mRNA levels and activities declined after EP withdrawal, while they were gradually increased by the continuous treatment with estradiol + MPA. In contrast, Mn-SOD mRNA levels and activities were not affected by EP withdrawal. IGFBP-1 mRNA levels were significantly increased 4 days after EP withdrawal and decreased thereafter, whereas they were gradually increased by the continuous treatment with estradiol + MPA. In conclusion, Cu,Zn-SOD, Mn-SOD and IGFBP-1 are differently regulated by estrogen and progesterone in human ESC. The decrease in Cu,Zn-SOD after the ovarian steroid withdrawal may be involved in endometrial breakdown.
endometrial stromal cell/estrogen/menstruation/progesterone/superoxide dismutase
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Introduction |
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Reactive oxygen species (ROS) and superoxide dismutase (SOD), an enzyme which scavenges superoxide radicals, play important roles in the regulation of endometrial function (Narimoto et al., 1990
; Sugino et al., 1996, 2000a, 2000b, 2001). The human endometrium has two types of SOD: copper–zinc SOD (Cu,Zn-SOD), located in the cytosol, and manganese SOD (Mn-SOD), located in the mitochondria (Sugino et al., 1996). Both SOD mediate a first enzymatic step that protects cells against toxic oxygen radicals. We have previously reported that Cu,Zn-SOD and Mn-SOD activities in the human endometrium are decreased and ROS are increased in the late secretory phase endometrium, just before menstruation, suggesting that the decrease in SOD activities may be involved in endometrial shedding by causing oxidative damage (Sugino et al., 1996). Withdrawal of ovarian steroids has been well accepted as a physiological stimulus for menstruation. Prostaglandin F2
(PGF2) and matrix metalloproteinase (MMP) have also been implicated as factors responsible for menstruation (Rodgers et al., 1994; Baird et al., 1996; Irwin et al., 1996; Marbaix et al., 1996), and increased activities of MMP and cyclooxygenase by withdrawal of ovarian steroids have been reported in the human endometrium (Schatz et al., 1994; Irwin et al., 1996; Marbaix et al., 1996; Salamonsen et al., 1997; Critchley et al., 1999). Therefore, it is of interest to know how endometrial SOD responds to the withdrawal of ovarian steroids. We have reported that SOD expression in human endometrial stromal cells (ESC) is induced by both estrogen and progesterone accompanied by decidualization in vitro and that the decline in SOD activities in the late secretory phase endometrium is prevented by administration of both estrogen and progesterone in vivo (Sugino et al., 2000a). However, it remains unknown how estrogen or progesterone affects SOD expression and whether the effect of estrogen or progesterone is associated with decidualization. The present study was undertaken to determine the effect of estrogen, progesterone, or the combination of both on SOD expression in human ESC and to investigate how SOD is affected in ESC by withdrawal of ovarian steroids. |
Materials and methods |
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This project was reviewed and approved by the committee of investigations involving human subjects of Yamaguchi University School of Medicine. Informed consent from the patient was obtained before collection of any tissue samples for this study.
Materials
Phenol Red-free Dulbecco's modified Eagle's medium (DMEM) and glutamine were purchased from ICN Biomedical Inc. (Aurora, OH, USA). Streptomycin, penicillin and 1xtrypsin–EDTA were from Life Technologies Inc. (Grand Island, NY, USA). Collagenase, estradiol and medroxyprogesterone acetate (MPA) were obtained from Sigma Chemical Co. (St Louis, MO, USA). Fetal calf serum (FCS) was from PAA Laboratories GmbH (Linz, Austria). Tissue flasks and nylon mesh were from Becton Dickinson Co. (Franklin Lakes, NJ, USA). Random hexamer and Taq DNA polymerase were from Perkin–Elmer Co. (Foster City, CA, USA). [-32P]Deoxycytidine triphosphate (dCTP) was from Amersham (Arlington Heights, IL, USA). Isogen was from Wako Pure Chemical Industries Ltd (Osaka, Japan).
ESC isolation
Human endometrium was obtained at hysterectomy from normally cycling pre-menopausal women, aged 29–42 years, who underwent surgery for myoma uteri or cancer of the uterine cervix. Endometrial samples were histologically diagnosed as late proliferative phase or early secretory phase according to published criteria (Noyes et al., 1950). Tissue samples were washed with Phenol Red-free DMEM containing 4 mmol/l glutamine, 50 µg/ml streptomycin and 50 IU/ml penicillin, and minced into small pieces of <1 mm3. ESC were isolated as reported previously (Sugino et al., 2000a). In brief, after the enzymatic digestion of minced tissues with 0.2% collagenase in a shaking water bath for 2 h at 37°C, stromal cells were separated by filtration through a 70 µm nylon mesh. The filtrates were washed three times, and the number of viable cells was counted by Trypan Blue dye exclusion. The homogeneity of the stromal cell preparation was verified by immunocytochemistry using the specific antibody against stromal cells, vimentin (data not shown). Cells were seeded at 105 cells/cm2 in 75 cm2 tissue culture flasks and incubated in Phenol Red-free DMEM containing glutamine, antibiotics and 10% dextran-coated charcoal-stripped FCS at 37°C, 95% air and 5% CO2. At confluence, cells were treated with 1xtrypsin–EDTA and subcultured into 25 cm2 tissue culture flasks. At ~80% confluence after the first passage, the cell culture medium was changed to the treatment medium.
Cell culture
We first examined the effect of estrogen, progesterone, or the combination of both on SOD activity and mRNA level in ESC. Cells were incubated with Phenol Red-free DMEM supplemented with glutamine, antibiotics, 2% stripped FCS (treatment medium) containing estradiol (10-8 mol/l), MPA (10-6 mol/l), or the combination of both for 18 days at 37°C, 95% air and 5% CO2. The concentrations of ovarian steroids and the period of incubation were based on our previous report (Sugino et al., 2000a). Second, we studied the effect of withdrawal of estradiol and progesterone (EP withdrawal) on SOD expression. ESC that had been treated with estradiol (10-8 mol/l) and MPA (10-6 mol/l) for 12 days were washed and then incubated with or without estradiol (10-8 mol/l) and MPA (10-6 mol/l) for a further 11 days at 37°C, 95% air and 5% CO2. Decidualization was confirmed by the mRNA expression of insulin-like growth factor-binding protein-1 (IGFBP-1), which is a specific marker of decidualization (Giudice et al., 1992; Kim et al., 1998; Sugino et al., 2000a). Three different experiments were performed in triplicate.
SOD assay
After incubation, cells were washed with PBS, resuspended in Tris–HCl buffer (0.01 mol/l, pH 7.4) and sonicated. Cu,Zn-SOD activity and Mn-SOD activity were determined as reported previously (Sugino et al., 1993). The amount of protein required for 50% inhibition in the absorbance at 550 nm was defined as one unit (nitrite unit = NU) of SOD activity. All data were expressed in NU of SOD activity per mg protein. Protein concentrations were determined by a published method (Lowry et al., 1951).
RT–PCR
Total RNA was isolated from the cultured cell with Isogen by the method provided by the manufacturer. For mRNA analysis, RT–PCR was performed with the oligonucleotide primers for Cu,Zn-SOD (5'-CGAGCAGAAGGAAAGTAATG-3' and 5'-TAGCAGGATAACAGATGAGT-3') and for Mn-SOD (5'-AGTTCAATGGTGGTGGTCATA-3' and 5'-CAATCCCCAGCAGTGGAATAA-3') as reported previously (Sugino et al., 2000a). Direct sequence analyses of the PCR products were performed for sequence verification (Sugino et al., 2000a). The oligonucleotide primers (5'-TGCTGCAGAGGCAGGGAGCCC-3' and 5'-AGGGATCCTCTTCCCATTCCA-3') were used for IGFBP-1 as a marker of decidualization (Kim et al., 1998; Sugino et al., 2000a). Two oligonucleotide primers (5'-CTGAAGGTCAAAGGGAATGTG-3' and 5'-GGACAGAGTCTTGATGATCTC-3') were also used to amplify ribosomal protein L19 mRNA as an internal control as reported previously (Chan et al., 1987). Briefly, 3 µg of total RNA was reverse-transcribed at 42°C in a reaction mixture (single-strength PCR buffer, 2.5 µmol/l deoxynucleotide triphosphate, 5 µmol/l random hexamer primer, 1.5 µmol/l MgCl2, and 200 IU Moloney murine leukaemia virus reverse transcriptase). The RT product was divided into two equal aliquots (one tube was for L19 primers), and PCR was performed. For PCR amplification, a mixture containing the oligonucleotide primers (50 pmol), [-32P]dCTP (2 mCi at 3000 Ci/mmol) and Taq DNA polymerase (2.5 IU) was added to each reaction. Amplification was carried out for 25 cycles consisting of 95°C (1 min), 52°C (1 min) and 72°C (1 min) for Cu,Zn-SOD, 25 cycles consisting of 95°C (1 min), 54°C (1 min) and 72°C (1 min) for Mn-SOD, and 24 cycles consisting of 94°C (1 min), 60°C (2 min) and 72°C (3 min) for IGFBP-1 followed by 10 min of final extension at 72°C in a programmed temperature control system PC-800 (ASTEC, Fukuoka, Japan). The predicted sizes of the PCR-amplified products were 455 bp for Cu,Zn-SOD, 282 bp for Mn-SOD, 379 bp for IGFBP-1 and 194 bp for L19. A linear curve was plotted using number of cycles of amplification versus densitometric values of the PCR products, measured with a BAS2000 (Fuji Photo Film Co., Tokyo, Japan). The optimal number of cycles for amplification within the linear range was chosen for each set of primers of SOD and L19 (data not shown). Reaction products were electrophoresed on an 8% polyacrylamide non-denaturing gel. After autoradiography, band intensities were analysed using a bioimaging analyser BAS2000. For quantification, the density of the signals of Mn-SOD, Cu,Zn-SOD and IGFBP-1 was normalized to that of the internal control L19.
Statistical analysis
Data were examined by analysis of variance and Duncan's new multiple range test. Differences were considered significant at P < 0.05.
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Results |
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The effect of estradiol and progesterone on Cu,Zn-SOD and Mn-SOD activities in human ESC is shown in Figure 1
. MPA significantly increased Cu,Zn-SOD activity and estradiol augmented this stimulatory effect of MPA whereas estradiol alone had no effect (Figure 1A). MPA also significantly increased Mn-SOD activity, and estradiol had no additive effect (Figure 1B). Figure 2 shows the effect of estradiol and progesterone on mRNA levels of Cu,Zn-SOD and Mn-SOD and of IGFBP-1, a specific marker of decidualization. MPA significantly increased mRNA levels of Cu,Zn-SOD and Mn-SOD, and estradiol had no effect on both SOD (Figure 2A and B). MPA significantly increased IGFBP-1 mRNA level and estradiol augmented this stimulatory effect of MPA whereas estradiol alone had no effect (Figure 2C).
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The effect of EP withdrawal on SOD activities in ESC is shown in Figure 3
. Cu,Zn-SOD and Mn-SOD activities were significantly increased by the pre-incubation with estradiol and MPA for 12 days (day 0), and further increased by the continuous treatment with estradiol and MPA [EP(+) group] (Figure 3). With EP withdrawal [EP(–) group], Cu,Zn-SOD activities gradually declined to the level of the control group without steroid treatment (Figure 3A). In contrast with Cu,Zn-SOD, Mn-SOD activities were not affected by EP withdrawal and increased in a manner similar to the EP(+) group (Figure 3B). Mn-SOD activities in the EP(–) group tended to be higher than those in the EP(+) group but there were no significant differences between them. Figure 4 shows Cu,Zn-SOD and Mn-SOD mRNA levels 11 days after EP withdrawal. Cu,Zn-SOD mRNA levels were significantly higher in the EP(+) group than in the control group whereas they were significantly decreased by EP withdrawal (Figure 4A). In contrast, Mn-SOD mRNA levels in the EP(–) group were not affected by EP withdrawal (Figure 4B). Changes in IGFBP-1 mRNA levels after EP withdrawal are shown in Figure 5. IGFBP-1 mRNA levels were significantly increased by the pre-incubation with estradiol and MPA for 12 days (day 0), and were further increased by the continuous treatment with estradiol and MPA [EP(+) group] (Figure 5). With EP withdrawal [EP(–) group], IGFBP-1 mRNA levels were significantly increased 4 days after EP withdrawal compared with the EP(+) group, but gradually decreased thereafter and were significantly lower than those in the EP(+) group 11 days after EP withdrawal.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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The present study showed that enzyme activities and Cu,Zn-SOD and Mn-SOD mRNA levels in human ESC are increased by progesterone treatment accompanied by the induction of IGFBP-1, a marker of decidualization. These changes in both SOD would not be due to the decidualization, because in spite of the transient increase in IGFBP-1 mRNA levels after the withdrawal of estradiol and progesterone, Cu,Zn-SOD activities were rapidly decreased while Mn-SOD activities were continuously increased. The present results also showed an additive effect of estradiol on the increase in Cu,Zn-SOD activities caused by progesterone, whereas there was no additive effect of estradiol on mRNA levels of Cu,Zn-SOD. Estradiol may thus act on a post-transcriptional pathway. However, estradiol had no additive effect on enzyme activities and Mn-SOD mRNA levels, and the additive effect of estradiol on IGFBP-1 mRNA levels was slight. Thus, further studies are needed to determine whether those additive effects of estradiol are biologically significant.
It is likely that Cu,Zn-SOD is under hormonal regulation, whereas there seem to be other factors besides progesterone regulating Mn-SOD. Although it is difficult to clearly explain the mechanism by which Mn-SOD activities still increased after the EP withdrawal, substances that stimulate Mn-SOD but not Cu,Zn-SOD may have been produced by ESC after EP withdrawal, e.g. cytokines such as tumour necrosis factor- (Tabibzadeh, 1996; Sugino et al., 1998). The gene promoters of both human Cu,Zn-SOD and Mn-SOD have the binding sites for glucocorticoid receptor/progesterone receptor (GR/PR) (Kim et al., 1994; Wan et al., 1994). These features may imply that progesterone can regulate both human Cu,Zn-SOD and Mn-SOD gene expression. However, there are many binding sites for other factors in the promoter regions of both SOD genes (Kim et al., 1994; Wan et al., 1994), suggesting the presence of complex molecular mechanisms modulating the expression of the Cu,Zn-SOD and Mn-SOD genes.
IGFBP-1 mRNA levels were up-regulated by progesterone and this effect was augmented by estradiol. These changes were similar to those in Cu,Zn-SOD activities; however, IGFBP-1 mRNA levels were transiently increased after EP withdrawal. The same response has been found in previous reports (Maslar et al., 1986; Chen et al., 1989; Zhu et al., 1990), in which production of prolactin, another marker of decidualization, was also transiently increased after progesterone withdrawal and decreased thereafter. These in-vitro findings seem to be consistent with a normal physiological change, that is the pseudodecidual change of human ESC occurring during the late secretory phase when serum progesterone and estradiol levels decrease. Although it is suggested that progesterone may have dual effects and that the balance between the stimulation and inhibition determines the overall prolactin production in ESC (Maslar et al., 1986; Zhu et al., 1990), further studies are needed to clarify the mechanism for the transient increase of IGFBP-1 after EP withdrawal.
Withdrawal of ovarian steroids has been well accepted as a physiological stimulus for menstruation. In the present study, EP withdrawal caused the decrease in Cu,Zn-SOD expression. This finding is consistent with our previous report showing that Cu,Zn-SOD activity in the human endometrium is lowest during the late secretory phase (Sugino et al., 1996). The decrease in SOD expression and activity by EP withdrawal may not only cause tissue damage but also produce substances such as PGF2 or MMP through ROS generation (Rodgers et al., 1994; Baird et al., 1996; Irwin et al., 1996; Marbaix et al., 1996). We have recently found that ROS stimulated PGF2 production in human ESC (Sugino et al., 2001), and also ROS have been reported to stimulate MMP activity (Owens et al., 1997; Buhimschi et al., 2000). Furthermore, decreased Cu,Zn-SOD activities are associated with increased concentrations of ROS and PGF2 in decidua of failed pregnancies (Sugino et al., 2000b). In fact, increases in PGF2 concentrations and MMP activities are observed in the late secretory phase endometrium (Downie et al., 1974; Maathuis and Kelly, 1978; Ishihara et al., 1986; Rodgers et al., 1994; Marbaix et al., 1995; Irwin et al., 1996), and activities of cyclooxygenase and MMP in the human endometrium are increased by progesterone withdrawal (Schatz et al., 1994; Irwin et al., 1996; Marbaix et al., 1996; Salamonsen et al., 1997; Critchley et al., 1999). Collectively, it seems possible that the decrease in Cu,Zn-SOD expression and activity by withdrawal of ovarian steroids causes ROS generation, which in turn induces menstruation by not only causing oxidative damage but also producing substances responsible for endometrial breakdown.
The present study may suggest that Cu,Zn-SOD and Mn-SOD play different roles in regulating ESC function because of their differential regulation after EP withdrawal. We have reported that Cu,Zn-SOD is closely related with the regulation of cell function, e.g. progesterone production in luteal cells (Sugino et al., 1993, 1998, 1999, 2000c), and PGF2 synthesis in decidual cells (Sugino et al., 2000b). On the other hand, Mn-SOD is an inducible type that can be responsive to inflammatory reactions or cytokines in rat luteal cells (Sugino et al., 1998) and in human ESC (A.Karube-Harada and N.Sugino, unpublished data), suggesting that Mn-SOD works protectively against rapidly induced oxygen radical cytotoxicity as reported previously (Wong and Goeddel, 1988; Wong et al., 1989). We therefore suggest that Cu,Zn-SOD plays important roles in the maintenance of cell function while Mn-SOD is necessary for cell survival.
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This work was supported in part by a grant from the UBE Foundation and Grant-in-Aid for Scientific Research (11671623 and 13671721) from the Ministry of Education, Science, and Culture, Japan.
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1 To whom correspondence should be addressed. E-mail: obgyn{at}po.cc.yamaguchi-u.ac.jp
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Submitted on April 17, 2001; accepted on October 5, 2001.
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