Molecular Human Reproduction, Vol. 7, No. 11, 1065-1072,
November 2001
© 2001 European Society of Human Reproduction and Embryology
Uterine physiology |
Induction of manganese superoxide dismutase by tumour necrosis factor-
in human endometrial stromal cells
Department of Obstetrics and Gynecology, Yamaguchi University School of Medicine, Minamikogushi 1-1-1, Ube 755-8505, Japan
Abstract
The present study was undertaken to investigate the effect of tumour necrosis factor-
(TNF) on superoxide dismutase (SOD) expression in human endometrial stromal cells (ESC) and to determine whether there is a difference in responsiveness to TNF between ESC and decidualized ESC. TNF increased manganese-SOD (Mn-SOD) mRNA level and Mn-SOD activity in a dose-dependent manner in ESC. The concentration of TNF required for an effect was lower for decidualized ESC than for non-decidualized ESC. TNF had no effect on copper-zinc-SOD (Cu,Zn-SOD) expression in either type of cell. Incubation of ESC with actinomycin D, an RNA synthesis inhibitor, blocked TNF-induced Mn-SOD mRNA expression, but cycloheximide, a protein synthesis inhibitor, had no effect. H7, an inhibitor of protein kinase C (PKC), also inhibited TNF-stimulated Mn-SOD mRNA expression in both types of cells. These findings suggest that TNF-induced Mn-SOD expression is regulated at the transcription level and mediated by PKC-dependent phosphorylation and that de-novo protein synthesis is not required for the TNF effect. In summary, TNF induces Mn-SOD expression in human ESC. This phenomenon may be important for protection of ESC from cytokine-mediated oxidative stress.
endometrial stromal cells/protein kinase C/superoxide dismutase/superoxide radical/TNF
Introduction
Superoxide radicals cause cell damage, whereas superoxide dismutase (SOD) protects cells by scavenging superoxide radicals. Eukaryotic cells have two types of cellular SOD: copper-zinc SOD (Cu,Zn-SOD), located in the cytosol, and manganese SOD (Mn-SOD), located in the mitochondria. Both types of SOD are expressed in human endometrium and play important roles in the regulation of human endometrial function (Narimoto et al., 1990
; Sugino et al., 1996, 2000a, b). In particular, SOD in human endometrial stromal cells (ESC) is increased with decidualization and is likely to contribute to the establishment and maintenance of pregnancy (Sugino et al., 1996, 2000a).
ESC are regulated by cytokines such as tumour necrosis factor-alpha (TNF) (Hunt et al., 1992; Inoue et al., 1994; Tabibzadeh et al., 1999). In human endometrium, ESC are often exposed to TNF from macrophages (Kamat and Isaacson, 1987; Klentzeris et al., 1992; Critchley et al., 1999) and endometrial epithelial cells and stromal cells (Tabibzadeh 1991; Hunt et al., 1992; Philippeaux and Piguet, 1993; Laird et al., 1996; Wolff et al., 1999). However, TNF causes superoxide radical generation and damages cells (Yamauchi et al., 1989, 1990; Zimmerman et al., 1989). Interestingly, it is reported that TNF-resistant cells produce Mn-SOD to protect themselves from the oxygen radical cytotoxicity by TNF (Wong and Goeddel, 1988; Wong et al., 1989). Therefore, it is important to understand how SOD expression responds in ESC exposed to TNF. The present study was undertaken to investigate the effect of TNF on Mn-SOD and Cu,Zn-SOD expression in ESC in vitro. Since the function of human ESC is influenced by decidualization (Huang et al., 1987; Higuchi et al., 1995; Sugino et al., 2000a), we further examined whether there is a difference in responsiveness to TNF between ESC and decidualized ESC.
Materials and methods
This project was reviewed and approved by the committee of investigations involving human subjects of Yamaguchi University School of Medicine, Japan. Informed consent was obtained from the patient before collection of any tissue samples for this study.
Reagents
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, medroxyprogesterone acetate (MPA), oestradiol, TNF, actinomycin D, cycloheximide and phorbol 12-myristate 13-acetate (TPA) were obtained from Sigma Chemical Co. (St Louis, MO, USA). 1-(5-isoquinoline sulphonyl)-2-methylpiperazine dihydrochloride [H-7, an inhibitor of protein kinase C (PKC)] was from Seikagaku Kogyo Co. (Tokyo, Japan). 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]deoxycitidine 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 patients with a normal menstrual cycle, aged 40–49 years, who underwent surgery for myoma uteri or early stage of cervical cancer. Endometrial samples were histologically diagnosed as the late proliferative phase according to published criteria (Noyes et al., 1950). Tissue samples were washed with Phenol Red-free DMEM containing 4mmol/l glutamine, 50 ug/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 with the medium, and the number of viable cells was counted by Trypan Blue dye exclusion. The homogeneity of the stromal cell preparation was verified by the immunocytochemistry for the stromal-reacting antibody (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 fetal calf serum (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 studied the effect of TNF on Mn-SOD and Cu,Zn-SOD expression in ESC. Cells were treated with test medium (Phenol Red-free and serum-free DMEM supplemented with glutamine and antibiotics) containing TNF (0.01, 0.1, 1 or 10 ng/ml) for 4 or 8 h at 37°C in an atmosphere of 95% air and 5% CO2. We then looked at whether decidualization affected responsiveness of ESC to TNF. To induce decidualization, ESC were incubated with Phenol Red-free DMEM supplemented with glutamine, antibiotics, 2% stripped FCS, MPA (10-6 mol/l), and oestradiol (10-8 mol/l) for 14 days at 37°C in 95% air and 5% CO2. The decidualized ESC were then incubated with TNF as described above. Decidualization was confirmed by expression of insulin-like growth factor-binding protein-1 (IGFBP-1) mRNA, which is a specific marker of decidualization (Giudice et al., 1992; Kim et al., 1998; Sugino et al., 2000a). To study the time course of the TNF effect, ESC and decidualized ESC were incubated with TNF (1 ng/ml) for 4, 6, 8 or 12 h under the conditions described above. Secondly, we examined whether the effect of TNF was dependent on gene transcription and whether de-novo protein synthesis was required for the TNF effect. For this purpose, ESC were incubated with TNF (1 ng/ml) in the presence or absence of actinomycin D (4 µmol/l), a potent RNA synthesis inhibitor, or cycloheximide (50 µmol/l), a protein synthesis inhibitor, for 4 h as described above. We further studied whether PKC was involved in the TNF effect. ESC were incubated with TPA (0.004, 0.04, 0.4 or 4 µmol/l) or TNF (1 ng/ml) in the presence or absence of H7 (0, 50 or 100 µmol/l), a PKC inhibitor, for 4 h as described above. A single incubation was performed in triplicate on cells from a single hysterectomy sample. The samples from three individuals were used in a single experiment. Therefore, three different incubations were performed in a single experiment. To examine the effect of TNF on cell viability, cells were seeded at 105 cells/ml into each well of a 24-well culture plate and incubated with TNF (1 ng/ml) for 12 h. After incubation, cells were collected by pipetting carefully and cell viability was tested by the Trypan Blue dye exclusion method. TNF had no effect on cell viability [before incubation: 93.6 ± 1.1%; 12 h-control: 86.8 ± 1.8%; 12 h-TNF (1 ng/ml): 85.3 ± 1.1%; mean ± SEM of three different experiments].
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 in the sonicated samples were determined as reported previously (Sugino et al., 1993). In brief, for total SOD activity, the sonicated sample was added in a reaction buffer containing hypoxanthine and preincubated for 5 min at 37°C. The mixture was then reacted with the enzyme solution containing xanthine oxidase for 30 min at 37°C, followed by the addition of colouring reagent. The final mixture was left for 30 min at room temperature and optical absorption was then measured at 550 nm. 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. For Mn-SOD assay, 2 mmol/l KCN was added in a reaction buffer. Cu,Zn-SOD activity was determined by subtracting Mn-SOD activity from the total 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).
Reverse transcription–polymerase chain reaction (RT–PCR)
Total RNA was isolated from the cultured cells 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 for IGFBP-1 (5'-TGCTGCAGAGGCAGGGAGCCC-3' and 5'-AGGGATCCTCTTCCCATTCCA-3') were used as markers 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 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 triphosphates, 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 µCi 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 for L19 and SOD transcripts (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 for Mn-SOD and Cu,Zn-SOD 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.
Results
The effect of TNF on Mn-SOD and Cu,Zn-SOD mRNA expression in ESC are shown in Figure 1A, B. TNF increased Mn-SOD mRNA levels in a dose-dependent manner, and TNF at 0.1 ng/ml significantly increased ESC Mn-SOD mRNA (Figure 1A). However, TNF had no significant effect on Cu,Zn-SOD mRNA levels (Figure 1B). Since the function of human ESC is influenced by decidualization (Huang et al., 1987, Higuchi et al., 1995; Sugino et al., 2000a), we further examined the effect of TNF on decidualized ESC. As shown in Figure 1C, the TNF concentration (0.01 ng/ml) required to increase Mn-SOD mRNA levels in decidualized ESC was lower than that required to increase Mn-SOD mRNA levels in non-decidualized ESC. TNF also had no significant effect on Cu,Zn-SOD mRNA levels in decidualized ESC (Figure 1D). Basal Mn-SOD activity levels were significantly (P < 0.05) higher in decidualized ESC (32.7 ± 7.4 NU/mg protein, mean ± SEM of three different experiments) than in non-decidualized ESC (11.8 ± 3.3 NU/mg protein) (Figure 2). TNF increased Mn-SOD activity in both ESC and decidualized ESC in a dose-dependent manner (Figure 2), and the concentration of TNF required to increase Mn-SOD activity was lower for decidualized ESC (0.1 ng/ml) than for non-decidualized ESC (1 ng/ml) (Figure 2). TNF had no significant effect on Cu,Zn-SOD activities in ESC or decidualized ESC (data not shown).
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The time course of changes in Mn-SOD mRNA levels and Mn-SOD activities in both ESC and decidualized ESC after treatment with 1 ng/ml TNF
are shown in Figures 3 and 4. TNF significantly increased Mn-SOD mRNA levels at all times studied in both ESC and decidualized ESC (Figure 3). Mn-SOD activity in decidualized ESC was higher than that in ESC at all times studied (Figure 4). TNF increased Mn-SOD activity in a time-dependent manner in both ESC and decidualized ESC (Figure 4).
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The increase in Mn-SOD mRNA levels induced by TNF
could reflect either increased transcription or increased stability of the message. To investigate whether the induction of Mn-SOD mRNA by TNF is dependent on gene transcription and to determine whether de-novo protein synthesis is required for the TNF effect, ESC were incubated with TNF in the presence or absence of actinomycin D, a potent RNA synthesis inhibitor, or cycloheximide, a protein synthesis inhibitor. As shown in Figure 5, actinomycin D completely abolished the stimulatory effect of TNF on Mn-SOD mRNA expression, but cycloheximide had no such effect (Figure 5). Actinomycin D or cycloheximide alone had no effect on Mn-SOD mRNA levels. The effects of actinomycin D and cycloheximide in decidualized ESC were similar to those in ESC (data not shown).
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Since PKC-dependent phosphorylation is involved in induction of Mn-SOD by TNF
(Fujii and Taniguchi, 1991; Suzuki et al., 1993), we first examined the effect of PKC activation on Mn-SOD mRNA levels in ESC. As shown in Figure 6A, TPA, an activator of PKC, increased Mn-SOD mRNA levels in a dose-dependent manner, whereas TPA had no significant effect on Cu,Zn-SOD mRNA levels (data not shown). The stimulatory effect of 0.04 µmol/l TPA was inhibited by H7, an inhibitor of PKC, in a dose-dependent manner and completely suppressed the effect at a concentration of 50 µmol/l (Figure 6B). H7 alone had no effect. The effects of TPA and H7 on Mn-SOD mRNA in decidualized ESC were similar to those in non-decidualized ESC (data not shown). The role of PKC in elevating Mn-SOD mRNA levels by TNF treatment was also examined. TNF significantly increased Mn-SOD mRNA levels, and this stimulatory effect of TNF was completely inhibited by H7 in both ESC and decidualized ESC (Figure 7).
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Discussion
The present study showed that human ESC responded to TNF to increase Mn-SOD expression. In the human endometrium, it has been reported that TNF is produced by endometrial epithelial cells (Laird et al., 1996; Tabibzadeh et al., 1999; Wolff et al., 1999), ESC (Tabibzadeh, 1991; Hunt et al., 1992; Popovici et al., 2000) and macrophages (Kamat and Isaacson, 1987; Klentzeris et al., 1992; Critchley et al., 1999). Recent evidence has shown that the receptor for TNF is also expressed in ESC (Popovici et al., 2000). Thus, ESC are exposed to TNF that causes superoxide radical generation and cell damage (Yamauchi et al., 1989, 1990; Zimmerman et al., 1989). ESC may protect themselves from TNF by inducing Mn-SOD expression since cytotoxic effects of cytokines can be reduced by increased levels of Mn-SOD (Wong and Goeddel, 1988). Furthermore, TNF-resistant cells produce Mn-SOD to protect themselves from the oxygen radical cytotoxicity by TNF (Wong and Goeddel, 1988; Wong et al., 1989). Thus, induction of Mn-SOD is likely to be important for survival of ESC.
In our present study, the Mn-SOD activity level in decidualized ESC was significantly higher than that in non-decidualized ESC, and this finding is consistent with our previously reported findings (Sugino et al., 2000a). In addition, our study suggested that responsiveness of ESC to TNF may be enhanced by decidualization because the concentration of TNF required to produce a response was lower in decidualized ESC than in non-decidualized ESC. This response may be due to the increase in TNF receptor because TNF receptor expression in ESC is up-regulated by decidualization (Popovici et al., 2000). These phenomena imply that the ability of ESC to scavenge superoxide radicals is increased by decidualization, and it seems to be compatible for the establishment and maintenance of pregnancy. We have reported that immunohistochemical expression of Mn-SOD in ESC increases during the late secretory phase and is further increased in decidual cells (Sugino et al., 1996).
Our study showed that PKC-dependent phosphorylation was likely to mediate induction of Mn-SOD expression by TNF. It has also been reported that TNF affected Mn-SOD expression via a PKC-mediated pathway in HeLa cells and endothelial cells (Fujii et al., 1991; Suzuki et al., 1993). In our study, the TNF-induced increase in Mn-SOD mRNA levels was completely abolished by the RNA synthesis inhibitor actinomycin D, whereas the protein synthesis inhibitor cycloheximide had no effect. These results suggest that the increase in Mn-SOD mRNA levels in ESC is dependent upon transcription and that de-novo protein synthesis is not required for the induction of Mn-SOD mRNA by TNF. The Mn-SOD promoter has numerous binding sites for transcription factors such as nuclear factor 
B (NFB), activating protein 1 (AP-1), promoter-selective transcription factor-1 (SP-1), and CCAAT/enhancer binding protein (C/EBP), which could mediate induction of Mn-SOD expression by TNF (Sen and Packer, 1996; Warner et al., 1996; Jones et al., 1997; Darville et al., 2000). It has been reported that TNF induces NFB activation via a PKC-independent pathway in human kidney cells (Daniel et al., 1995). However, PKC may be involved in SP-1-induced Mn-SOD expression in endothelial cells (Tanaka et al., 2000). Further studies are needed to determine which transcription factors are involved in PKC-mediated Mn-SOD induction by TNF.
Our study showed that Mn-SOD was selectively induced by TNF, suggesting that Mn-SOD and Cu,Zn-SOD play different roles in regulating the function of human ESC. In general, Cu,Zn-SOD is expressed constitutively, whereas Mn-SOD is inducible and can be responsive to inflammatory reactions or cytokines (Sugino et al., 1998). Differential regulation of Mn-SOD and Cu,Zn-SOD also occurs during inflammatory responses involving ovulation (Sato et al., 1992), corpus luteum regression (Sugino et al., 1998, 2000c), and in decidua of failed pregnancy (Sugino et al., 2000b). We postulate that Cu,Zn-SOD constitutively scavenges superoxide radicals, whereas Mn-SOD is rapidly induced by inflammation and is necessary for cell survival during rapid superoxide radical generation (Sugino et al., 1996, 1998, 1999, 2000b,c; Suzuki et al., 1999).
Acknowledgements
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.
Notes
1 To whom correspondence should be addressed. E-mail: obgyn{at}po.cc.yamaguchi-u.ac.jp 
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Submitted on April 18, 2001; accepted on August 24, 2001.
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