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RESEARCH |
Faculté de Médecine Vétérinaire, Centre de Recherche en Reproduction Animale (CRRA), Université de Montréal, St-Hyacinthe, Québec, Canada J2S 7C61 Laboratory of Ontogeny and Reproduction, Pavillon CHUL, Ob/Gyn Department, Faculty of Medicine, Centre Hospitalier Universitaire de Québec (CHUQ), Centre de Recherche en Biologie de la Reproduction (CRBR), Laval University, Québec City, Québec, Canada G1V 4G2
Correspondence should be addressed to P D Carrière; Email: paul.d.carriere{at}umontreal.ca
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Abstract |
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-glutathione S-transferase (GSTA), but inhibited the amount of steroidogenic acute regulatory protein (STAR) mRNA. Conversely, P4 and mRNA expression of STAR, cytochrome P450 side-chain cleavage (CYP11A1), HSD3B, and GSTA increased with time in culture. TGFB1 inhibited P4 secretion and decreased mRNA expression of STAR, CYP11A1, HSD3B, and GSTA. TGFB1 modified the formation of granulosa cell clumps and reduced total cell protein. Finally, TGFB1 decreased conversion of androgens to E2, but did not decrease the conversion of estrone (E1) to E2 and pregnenolone to P4. Overall, these results indicate that TGFB1 counteracts stimulation of E2 and P4 synthesis in granulosa cells by inhibiting key enzymes involved in the conversion of androgens to E2 and cholesterol to P4 without shutting down HSD17B reducing activity and HSD3B activity. |
Introduction |
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Gonadotropin stimulation of responsive follicles is associated with increased synthesis of estradiol-17β (E2) and progesterone (P4), the two key steroid hormones associated with the development of the ovulatory follicle (Price et al. 1999, Kolibianakis et al. 2005). E2 is produced by granulosa cells and is important for granulosa cell growth, attenuation of granulosa cell apoptosis, and positive and negative feedback regulation of the hypothalamic–pituitary–ovarian axis (Kolibianakis et al. 2005). In ruminants and humans, gonadotropin stimulation of E2 requires luteinizing hormone (LH) stimulation of theca cells to produce androgens, mostly as androstenedione (A4), and follicle-stimulating hormone (FSH)-mediated conversion of theca-derived A4 to E2 in granulosa cells (Fortune 1986, Hillier et al. 1994). A4 is converted to estrone (E1) by cytochrome P450 aromatase (CYP19A1) and then into E2 by 17β-hydroxysteroid dehydrogenase (HSD17B) reducing enzymes (Hillier et al. 1994, Mindnich et al. 2004). Granulosa cells also produce P4, which is necessary for the induction of ovulation (Drummond 2006). The production of P4 involves transformation of cholesterol to pregnenolone (P5) by the cytochrome P450 side-chain cleavage (CYP11A1) followed by the conversion of P5 to P4 by 3β-hydroxysteroid dehydrogenase (HSD3B). In addition, -glutathione S-transferase (GSTA) is expressed in bovine granulosa cells and codes for a protein with high HSD3B activity (Rabahi et al. 1999, Raffalli-Mathieu et al. 2007). In vivo, most of the steroidogenic enzyme genes are not expressed in granulosa cells of small bovine antral follicles (0.4–4 mm; Bao & Garverick 1998). In granulosa cells, expression of CYP19A1 and CYP11A1 gradually increases during follicle growth, and HSD3B is first observed in non-atretic follicles at 
8 mm (Xu et al. 1995, Bao et al. 1997). These data indicate that the timely expression of steroidogenic enzymes at distinct periods of follicular development is important for the selection of the dominant follicle and successful ovulation. A better characterization of the regulation of E2 and P4 synthesis in granulosa cells will improve our understanding of follicle development.
In recent years, much attention has focused on the role of the members of the transforming growth factor-β (TGFB) superfamily acting as paracrine and autocrine factors to modulate ovarian function and fertility (Knight & Glister 2006). TGFB1, which is the most extensively studied factor of this family, is present in granulosa and theca cells and in the vascular system of the ovary in many species (Nilsson et al. 2003, Juengel & McNatty 2005), and has been shown to either stimulate or inhibit E2 and P4 synthesis. For instance, TGFB1 stimulated E2 and P4 secretion from rodent granulosa cells (Zachow et al. 1999, Knight & Glister 2006), whereas TGFB1 inhibited granulosa cell secretion of E2 and P4 from pigs and ruminants (Chang et al. 1996, Wandji & Fortune 1996, Ford & Howard 1997, Juengel et al. 2004, Ouellette et al. 2005). These reports detailing the effect of TGFB1 on ovarian cells appear to be highly dependent on the species studied, stage of follicle differentiation, and the presence of different growth factors as co-treatments, and the mechanism of TGFB1 action in granulosa cells is not clear. In vivo, the complexities of hormonal interactions with the cytokines produced by ovarian cells limit our investigations of steroidogenesis in follicle development. Fortunately, E2 secretion can be maintained for several days in bovine granulosa cells cultured in vitro with FSH in serum-free conditions (Gutierrez et al. 1997). This in vitro model mimics the gradual increase in E2 secretion seen in the growing follicles and can be used to identify the key factors regulating steroidogenesis in granulosa cells. Therefore, the objective of the present study was to determine the effect of TGFB1 on E2 and P4 synthesis and the corresponding expression and activity of key steroidogenic enzymes in FSH-stimulated bovine granulosa cells.
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Results |
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Discussion |
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In developing antral follicles, a positive E2/P4 ratio must be maintained and it is critical to limit P4 secretion until the time of ovulation induction, because premature increase in P4 is associated with follicular atresia (Ireland & Roche 1982, Irving-Rodgers et al. 2003). In agreement with the above, a low dose of FSH stimulated E2 but not P4 in the present study and CYP11A1 was only stimulated by the highest dose of FSH (10 ng/ml). Additionally, the present study is the first report showing that FSH down-regulates the expression of STAR in vitro. This finding may explain why STAR is undetectable in the granulosa of healthy antral follicles at any size in vivo (Soumano & Price 1997, Bao et al. 1998). In our time-course experiments, in the presence of low dose of FSH, the production of P4 increased as well as the expression of STAR, CYP11A1, HSD3B, and GSTA. These findings are in agreement with a previous study (Sahmi et al. 2004), which showed an increase with time in HSD3B and CYP11A1. Overall, these results indicate that P4 increases spontaneously in cultured granulosa cells and that readily available stores of cholesterol are present in granulosa cells, which can be transformed to P4 by CYP11A1, HSD3B, and GSTA. Similar to the effect of TGFB1 on E2 synthesis, TGFB1 also inhibited the progestin synthetic pathway. TGFB1 inhibited P4 secretion and abundance of mRNA encoding STAR, CYP11A1, HSD3B, and GSTA, which are required for sustained production of P4 from cholesterol. These data are consistent with the effects of TGFB1 on STAR, CYP11A1, and HSD3B in thecal, adrenocortical, and adrenal tumor cells among different species (Rainey et al. 1991, Cherradi et al. 1995, Naaman-Reperant et al. 1996, Attia et al. 2000, Herrmann et al. 2002), and this is the first time that TGFB1 has been shown to inhibit mRNA encoding GSTA. Surprisingly, despite the reduced abundance of HSD3B and GSTA mRNA, TGFB1 did not affect total HSD3B activity. Similarly, TGFB1 did not significantly alter HSD3B activity in the rat fetal testis (Gautier et al. 1997). TGFB1 may have stabilized the corresponding enzyme proteins of HSD3B and GSTA or, alternatively, other unknown gene products with HSD3B activity may be involved.
In agreement with previous morphological studies (Gutierrez et al. 1997, Marsters et al. 2003), FSH increased cell number. In this model, it has been suggested that after dispersion, granulosa cells revert to a less mature phenotype, re-establish cell–cell communications, and proliferate in the presence of FSH (Gutierrez et al. 1997, Marsters et al. 2003). The moderate increase in total cell protein observed in the presence of FSH could indicate that FSH stimulated proliferation or, alternatively, that FSH prevented apoptosis and increased cell survival. FSH and E2 are known to act as survival factors to induce granulosa cell proliferation and prevent apoptosis (Gutierrez et al. 1997, Yang & Rajamahendran 2000, Jiang et al. 2003, Quirk et al. 2004). In the present study, TGFB1 caused visible differences in the morphology of granulosa cell clumps, which appeared smaller and more spherical than those in FSH-treated controls. TGFB1 at the highest dose also caused a slight decrease in total granulosa cell protein. It is unclear at the present time whether the TGF-induced reduction in steroidogenesis is a result or cause of the change in cell proliferation or survival. But, in the absence of FSH, TGFB1 did not significantly affect total granulosa cell protein. Similarly, TGFB1 alone had no effect on DNA synthesis in cultured bovine granulosa cells (Lerner et al. 1995). Therefore, the effects of TGFB1 on granulosa cells could be due to inhibition of the cell-surviving activity of FSH and/or mediated through a loss of E2-stimulated cell survival (Yang & Rajamahendran 2000, Quirk et al. 2004). Ongoing experiments in our laboratory will test this hypothesis, by investigating the effects of TGFB1 on proliferation and apoptosis of bovine granulosa cells cultured with or without FSH.
We conclude that TGFB1 plays an inhibitory role in E2 and P4 steroidogenesis in granulosa cells cultured in conditions where E2 and P4 secretion is being stimulated, and that TGFB1 counteracts the stimulation of mRNA encoding steroidogenic enzymes. As TGFB1 inhibited FSHR mRNA levels and inhibited FSH-induced CYP19A1 and HSD17B1 but not HSD17B7, we propose that the inhibitory effects of TGFB1 on FSH-stimulated E2 secretion may be due at least in part to the inhibition of FSHR (Fig. 8). These selective inhibitory effects suggest that TGFB1 may be acting in a physiological manner to limit the amount of E2 and P4 produced by the granulosa cells without totally shutting down the steroidogenic potential (i.e., HSD17B reducing activity and HSD3B activity are unaffected). By acting in this manner, the physiological role of TGFB1 may be to limit FSH-stimulated growth and differentiation of granulosa cells and play an active role in determining the fate of the developing follicle toward ovulation or atresia.
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Materials and Methods |
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Cell culture
Cell culture was performed essentially as described by Gutierrez et al. (1997). Briefly, ovaries were collected at a local abattoir from adult cows irrespective of the stage of the estrous cycle and transported to the laboratory at 37 °C in PBS containing penicillin (100 IU/ml), streptomycin (100 µg/ml), and fungizone (1 µg/ml). Follicles of 2–5 mm in diameter were dissected from the ovaries, and granulosa cells were isolated mechanically by rinsing sections of follicle walls repeatedly through a disposable pipette. The granulosa cell suspension was filtered through a 150 mesh steel sieve (Sigma) to remove oocytes.
The cells were seeded onto 24-well tissue culture plates (Corning Glass Works, Corning, NY, USA) at a density of 106 viable cells (tested by Trypan blue exclusion) in 1 ml -MEM with L-glutamine containing sodium bicarbonate (10 mM), HEPES (20 mM), non-essential amino acid mix (1.1 mM), penicillin (100 IU/ml) and streptomycin (100 µg/ml), protease-free BSA (0.1%), sodium selenite (4 ng/ml), transferrin (2.5 µg/ml), A4 (100 nM; all from Sigma), ovine FSH (1 ng/ml; oFSH, AFP-5332B; NIDDKD, Torrance, CA, USA), insulin (10 ng/ml; Invitrogen), and graded doses of recombinant active human TGFB1 (R&D Systems, Minneapolis, MN, USA) starting on the first day of culture. Cultures were maintained at 37 °C in 5% CO2 for 6 days, with 700 µl medium being replaced every 2 days.
At the end of culture, the medium was collected and frozen for subsequent steroid assay and granulosa cells were collected for RNA extraction or lysed for total protein measurement. Total cell protein was extracted by the addition of 200 µl of 1 M NaOH to each well for 2 h at room temperature, followed by neutralization with 200 µl of 1 M HCl. Protein concentrations were measured using the Bio-Rad micro-assay (Bio-Rad). All experiments were performed with at least three independent cell cultures, and three to five wells per treatment were pooled for each assay.
Steroid assays
Culture medium samples were assayed for E2 as reported previously (Bélanger et al. 1990), but without C-18 column extraction. Cross-reaction of A4 and E1 with the E2 assay was less than 0.1% (Bélanger et al. 1980). P4 was measured in duplicate as described (Lafrance & Goff 1985). Intra- and inter-assay coefficients of variation were less than 15% for both assays. The sensitivity of the E2 and P4 assays was 8 and 32 pg per tube respectively. The steroid hormone concentrations were corrected for cell number by normalization to total cell protein per well.
RT-PCR
Total RNA was extracted using the RNeasy kit (Qiagen), according to the manufacturer's instructions, and treated with DNase (Qiagen). The RT reaction was performed on 1 µg total RNA with Omniscript enzyme (Qiagen). Gene expression was measured by semi-quantitative PCR. The primers used were those described previously for cyclophilin (1B15; Bettegowda et al. 2006), CYP11A1 (Vanselow et al. 2004), HSD3B (Vanselow et al. 2004), CYP19A1 (Sahmi et al. 2004), and FSHR (Ndiaye et al. 2005). Sense (5'-TTGTGCGAGAGTCTGGCGATTCT-3') and antisense (5'-AGGAATCGCTCGGTGGTGAAGTA-3') primers for HSD17B1 were designed based on the bovine sequence (NM_001102365) with a product size of 287 bp. Sense (5'-CGGTTGCTGGAAGAAGATGATG-3') and antisense (5'-TCACCAGAGGATTGAGAGACTCG-3') primers for HSD17B7 were designed based on the bovine sequence (XM_581467) with a product size of 789 bp. Sense (5'-GACACGGTCATCACTCACGAGTT-3') and antisense (5'-ATGCTGAGCAGCCAGGTGAGTT-3') primers for STAR were designed based on the bovine sequence (XM_001250261) with a product size of 248 bp. Sense (5'-GAATGGAGTGCATTCGGTGGCTC-3') and antisense (5'-GACTGCTGACTCTGGCTTTTAGG-3') primers for GSTA were designed based on the bovine sequence (BTU49179) with a product size of 528 bp. Forward and reverse primers used in the PCRs were located in different exons to avoid amplification of any residual genomic DNA. The PCR products for each gene were sequenced to confirm the identity of the gene. PCR was performed under the following conditions: (1) initial denaturation at 94 °C for 3 min; (2) amplification cycles of denaturation at 94 °C for 45 s, annealing for 45 s at 60 °C (CYP11A1, HSD3B, and FSHR) or 64 °C (HSD17B1, HSD17B7, GSTA), or for 30 s at 62 °C (STAR, 1B15 and CYP19A1); (3) elongation at 72 °C for 1 min; and (4) final elongation at 72 °C for 5 min. Optimal cycle number for amplification during the exponential phase was determined for each gene. The reactions were performed for 31 cycles for STAR, 35 cycles for CYP11A1, 34 cycles for HSD3B, 25 cycles for GSTA, 29 cycles for CYP19A1, 36 cycles for HSD17B1 and HSD17B7, 37 cycles for FSHR, and 27 cycles for 1B15. The PCR products were separated on 2% agarose gels containing 0.001% ethidium bromide and visualized under u.v. light. Quantification of band intensity was performed with NIH Image J software (http://rsb.info.nih.gov/nih-image/). Target gene mRNA abundance was expressed relative to 1B15 mRNA abundance.
Enzyme activity assays
Short-term incubation of tritiated steroid hormone precursors was conducted at the end of day 6 of culture to measure specific enzyme activities. On day 6, all the medium of each well was removed and replaced with fresh medium without A4 but containing 6–11 nM (corresponding to 1.6x106 disintegrations per minute (DPM)/ml medium) of either [3H]E1, [3H]A4, [3H]T, or [3H]P5 and 0, 0.1, or 0.5 ng/ml TGFB1. Cells were incubated for 1.5 or 3 h at 37 °C. At the end of the incubation, the medium was recovered and frozen at –20 °C until analysis of steroid metabolism by thin layer chromatography (TLC) as described previously (Godin et al. 1999). Briefly, steroids were extracted from the medium using diethyl ether and resolved on DC-Alufolien neutral (type E) paper plates (Whatman, Maidstone, Kent, England) in toluene:acetone (4:1). Each TLC plate contained [3H]E1, [3H]E2, [3H]A4, [3H]T, and [3H]P5 as standards. A culture medium control was performed by incubating tracer in culture medium without cells, and was used to obtain background radioactivity that was subtracted from product counts. After migration of samples, the TLC plates were exposed to phosphor screens designed for tritium detection, and tritiated steroid metabolites were localized with a Storm 840 Phosphorimager (Molecular Dynamics, Sunnyvale, CA, USA). The rate of production of specific steroid metabolites was quantified by scraping the corresponding sample and background spots from the TLC plate and counting the radioactivity using PCS scintillation fluid (Amersham).
Activity assays were validated by determining the conditions required to maintain excess substrate. In preliminary time-course experiments, 1.6x106 DPM of [3H]precursor (6–11 nM) were incubated with granulosa cells for 3 and 6 h. The amount of conversion of [3H]A4 and [3H]T precursors to [3H]E2 was similar with 29 and 58% conversion after 3 and 6 h respectively, and thus an incubation time of 3 h was selected to measure the rate of conversion of [3H]A4 and [3H]T to [3H]E2. For HSD17B reducing activity, the amount of conversion of [3H]E1 precursor to [3H]E2 was 92 and 98% after 3 and 6 h respectively. Therefore, to obtain experimental conditions of excess precursor, increasing concentrations of unlabeled E1 (10–7, 10–6, 10–5 M) were added to the 8.8 pmol/ml of [3H]E1, and incubation time was reduced to 1.5 h. This resulted in 6, 20, and 30% conversion of [3H]E1 to [3H]E2 respectively, and therefore 10–6 M unlabeled E1 was added to all [3H]E1 incubations to quantify HSD17B reducing activity. For HSD3B activity, the amount of conversion of [3H]P5 precursor to [3H]P4 was 37, 69, 79, and 90% conversion after 1.5, 3, 4.5, and 6 h respectively, and thus an incubation time of 1.5 h was selected to measure the rate of conversion of [3H]P5 to [3H]P4.
Statistical analysis
Statistical analysis was performed using the JMP software (SAS Institute, Cary, NC, USA). Data are presented as means±S.E.M. The data were normally distributed as verified using the Shapiro–Wilk test. One-way ANOVA was used to test the main effect of FSH, time, and TGFB1 on the measured parameters. Differences between treatment dose of FSH or TGFB1 with the 0 dose control or between 4- and 6-day cultures with the 2-day culture group were identified with Dunnett's test.
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Declaration of interest |
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Funding |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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Acknowledgements |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestFundingAcknowledgementsReferences |
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Received 9 July 2007
First decision 7 September 2007
Revised manuscript received 2 July 2008
Accepted 17 July 2008
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References |
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